REVIEW article

Front. Environ. Sci., 31 July 2024

Sec. Toxicology, Pollution and the Environment

Volume 12 - 2024 | https://doi.org/10.3389/fenvs.2024.1397850

Exploring bioremediation strategies for heavy metals and POPs pollution: the role of microbes, plants, and nanotechnology

  • 1. School of Bioengineering and Biosciences, Lovely Professional University, Phagwara, Punjab, India

  • 2. Indian Institute of Technology, Roorkee, Uttrakhand, India

  • 3. School of Agricultural Sciences, Baddi University of Emerging Sciences and Technologies, Baddi, Himachal Pradesh, India

  • 4. Department of Biological Sciences, Al Hussein Bin Talal University Ma’an, Ma’an, Jordan

  • 5. Department of Biomedical Sciences, Institute of Health, Jimma University, Jimma, Ethiopia

Abstract

Heavy metal and Persistent Organic Pollutants (POPs) pollution stemming from industrialization, intensive agriculture, and other human activities pose significant environmental and health threats. These contaminants persist in the air, soil, and water, particularly in industrialized nations, adversely affecting human health and ecosystems. While physical and chemical methods exist for detoxifying contaminated soil, they often have drawbacks such as high cost and technical complexity. Bioremediation, utilizing plants and microbes, offers a promising solution. Certain microorganisms like Streptomyces, Aspergillus and plant species such as Hibiscus and Helianthus show high metal adsorption capacities, making them suitable for bioremediation. However, plants’ slow growth and limited remediation efficiency have been challenges. Recent advancements involve leveraging plant-associated microbes to enhance heavy metal removal. Additionally, nanotechnology, particularly nano-bioremediation, shows promise in efficiently removing contaminants from polluted environments by combining nanoparticles with bioremediation techniques. This review underscores bioremediation methods for heavy metals using plants and microbes, focusing on the role of Plant Growth Promoting Rhizobacteria (PGPR) in promoting phytoremediation. It also explores the implementation of nanotechnologies for eliminating metals from polluted soil, emphasizing the significance of soil microbiomes, nanoparticles, and contaminant interactions in developing effective nano-remediation strategies for optimizing agriculture in contaminated fields.

1 Introduction

Plenty of biochemical interactions in plants and animals require heavy metals (HMs), making them essential to manufacturing. When present in high concentrations, these heavy metals (HMs)/pollutants can disrupt essential metabolic activities in living beings, which makes them severely harmful pollutants in ecologically vulnerable regions (Ding et al., 2022; Mustapha and Halimoon, 2022). Natural disasters like volcanic eruptions and human activity have also contributed to this pollution of the environment. Municipal garbage, agricultural waste, and industrial activities like mining and electroplating all contain high amounts of heavy metals like lead (Pb), mercury (Hg), zinc (Zn), copper (Cu), cadmium (Cd), nickel (Ni), cobalt (Co), and chromium (Cr) (Hananingtyas et al., 2022; Mitra et al., 2022). Even though heavy metals, unlike organic materials, do not naturally degrade, the toxicity of heavy metals can be reduced through several different mechanisms, one of which is bioremediation (Kumar et al., 2022). Bioremediation has emerged as the most popular and effective solution for treating metal-polluted locations. Bioremediation refers to employing microorganisms to break down harmful contaminants in soil or water into less hazardous byproducts (Riyazuddin et al., 2022; Vanisree et al., 2022; Zaynab et al., 2022).

Plants (phytoremediation) (Gavrilescu, 2022) and microorganisms (rhizo-remediation) (Husain et al., 2022) working together in the root zone are crucial components of biological remediation (Sharma et al., 2021; Cepoi et al., 2022; Pande et al., 2022). Both in-situ and ex-situ technologies may be employed, depending on the specificity of the contaminated area. In-situ technologies are used for passive, non-invasive clean-up, while ex-situ technologies are used for cost-effective and safe clean-up (Sharma et al., 2021). In In-situ biodegradation, naturally occurring microorganisms are prompted to break down organic pollutants by supplying nutrients and oxygen via the uniform circulation of aqueous solutions extracted from soil containing hazardous heavy metals (Reddy and Parupudi, 1997). Groundwater and soil both respond well to in-situ bioremediation. Several bioremediation techniques, such as land farming and composting, are employed in ex-situ bioremediation (Concetta et al., 2013; ; Tufail et al., 2022), which entails the removal of contaminated soil from its original location. Table 1 outlines various in-situ and ex-situ bioremediation techniques employed for the effective removal of heavy metals and persistent organic pollutants (POPs), showcasing diverse methods essential in addressing environmental contamination challenges.

TABLE 1

CategoryTechniqueDescriptionAdvantagesDisadvantages
In-SituIntrinsic bioremediation (natural attenuation)Relies on naturally occurring microbes in the environment to degrade or immobilize metals.Low cost, minimal disruptionSlow process, limited control over remediation rate
BiostimulationEnhances the growth and activity of indigenous microbes by adding nutrients (e.g., phosphorus, nitrogen) and oxygen.Faster than intrinsic bioremediation, utilizes existing microbial populationsMay require long-term maintenance, potential for unintended consequences
BioaugmentationIntroduces specially selected or engineered microbes to degrade or immobilize metals.Faster and more targeted than biostimulation, applicable to sites with limited microbial populationsExpensive, risk of introducing invasive species
BioventingInjects air into the contaminated soil to stimulate aerobic degradation and volatilization of some metals.Effective for volatile metals, low energy consumptionLimited to specific metals, can spread volatile contaminants
BiospargingInjects air or other gases (e.g., methane) under pressure to enhance biodegradation and desorption of metals.Faster and more targeted than bioventing, applicable to deeper contaminationExpensive, requires specialized equipment
PhytoremediationUses metal-accumulating plants (hyperaccumulators) to extract and concentrate metals in their tissues.Sustainable, aesthetically pleasing, applicable to large areasSlow process, limited to bioavailable metals, requires proper plant management
Ex-SituLandfarmingSpreads contaminated soil over a prepared bed and stimulates microbial degradation through aeration and nutrient addition.Relatively low cost, simple to operateRequires large land area, potential for contaminant dispersal
CompostingMixes contaminated soil with organic bulking agents (e.g., manure, compost) to stimulate microbial degradation at high temperatures.Effective for organic contaminants along with metals, creates useable compost productRequires controlled conditions, potential for odor problems
BioreactorsTreats contaminated soil or water in a controlled environment with optimized conditions for microbial growth and degradation.Highly efficient, fast treatment timesExpensive, complex to operate, requires transportation of contaminated material

In-situ and Ex-situ bioremediation techniques used for remediation of heavy metals and POPs (RoyChowdhury et al., 2018; DalCorso et al., 2019; Ravindra and Mor, 2019; Zwolak et al., 2019; Sharma et al., 2021; Cepoi et al., 2022; Pande et al., 2022).

Various variables and factors in bioremediation, including electron acceptors, soil type, nutrients, oxygen presence, temperature, and pH, play an important role (Zhai et al., 2018). They can thrive in various temperatures and humidity levels, and microbes are extensively versatile for these environmental conditions. The versatility of microbes and other biological agents makes them capable of removing or remediating heavy metal pollutants in the environment. However, a deeper understanding of microbial ecology and bioremediation methods is essential to fully harness their potential. While enhancing bioremediation processes holds promise, the intricate interactions between microorganisms and heavy metal contamination can present challenges that may impede successful outcomes (Jabbar et al., 2022). Several methods, like protein engineering, whole-transcriptome profiling, metabolic engineering, and rhizo-remediation, can aid bioremediation by improving heavy metal binding for detoxification and xenobiotic chemical degradation. For example, genetically altered Deinococcus geothermalis expressed the mer-operon responsible for reducing Hg (II) after being inserted from Escherichia coli. This allowed the bacteria to reduce Hg (II) contamination (). In addition, the gram-negative strain of Ralstonia eutropha underwent genetic engineering to express a mouse protein known as metallothionein on the cell surface. This rendered the strain resistant to heavy metals (Valls et al., 2000), and when added to Cadmium-contaminated soil, bacteria have shown a significant improvement in tobacco plant growth.

2 Heavy metal and POPS pollution: threats to soil health, plant growth, and human wellbeing

Polluting the environment is a major problem that has emerged as a major obstacle in the modern world. Heavy metals (about 65) pose the greatest environmental concern (Tufail et al., 2022). Metals with densities of more than 5 g/cm3, known as “heavy metals,” are one of the world’s greatest dangers because of their widespread discharge into the environment (Roy et al., 2018; DalCorso et al., 2019; Ravindra and Mor, 2019; Zwolak et al., 2019). Various metals and metalloids like Cr, Cd, Cu, Pb, Zn, Ni, Hg, and As are discharged into the environment through sewage disposal, smelting, fertilizer applications, and industrial waste (Zwolak et al., 2019; ; Sall et al., 2020). The available evidence indicates that a majority, exceeding 50%, of the total 10 million contaminated sites, equivalent to a land area exceeding 20 million hectares, are found to be contaminated with these substances (RoyChowdhury et al., 2018). A few HM concentrations available in soil are mentioned in Table 2.

TABLE 2

HMsAvailable min. amount in soil (mg/kg)Available max. amount in soil (mg/kg)
Pb0.169,000
Zn0.357,012
Mn3.042,600
Cr0.0510,000
Ni05,000
Hg01,800
Cu0.11,790
Cd01,458
As0.1253

Heavy metal minimum and maximum concentrations in soil documented worldwide (shorted as per Maximum concentration) (Saleem et al., 2022).

Adsorption and desorption affect the availability of these metals in soil; these processes are, in turn affected by a wide range of soil parameters, including calcium carbonate, clay mineral, oxidation-reduction status, cation exchange, organic matter content, pH, Mn, and Fe oxide concentrations (Islam et al., 2017; Chen and Li, 2018; Sall et al., 2020). As a result of these factors, there is a range of heavy metal types and concentrations present in soils across diverse agro-climatic regions, each with its unique features and functions. The persistent, bioaccumulative, and inert nature of these metals in the soil-plant system contributes to complex issues related to their toxicity and long half-life (Wang Q. et al., 2018). Two significant issues are predicted to arise due to heavy metal accumulation in soils: i) a decrease in soil nutrition due to changes in the microbiota (Xie et al., 2016) and ii) a decrease in human health through plants and the food chain at and near contaminated locations (Zwolak et al., 2019). Besides causing damage to the soil, even low levels of metals can pose a significant risk to plant ecosystems due to their strong reactivity. Therefore, it is essential to swiftly comprehend how metals interact with the soil, microbiome, and plants’ systems to enhance crop yields in stress-prone soils. Moreover, affordable approaches to stress management should be devised. To prevent and eliminate metal pollution, stringent regulations must be enforced by the government or private entities, and detoxification procedures must be implemented to regulate the release of heavy metals from various sources (; Liu et al., 2019; Dhaliwal, Singh, Taneja and Mandal, 2020). Removing heavy metals relies on or follows the regulatory standards set for soil heavy metal levels in numerous countries. These criteria can differ from one location to another and vary depending on the specific type of heavy metal in question. Also, such standards aid in developing more effective solutions for removing heavy metals from contaminated locations (Zhan et al., 2019). This review will briefly describe the toxic effects of a few metal pollutants on plants and microorganisms and how these effects can be mitigated. From a biological point of view, HMs can be broken down into two categories: necessary and harmful (Ullah et al., 2022). Micronutrients for plants and animals are called “essential metals” or “metalloids” and include elements like zinc, iron, nickel, and copper (Manoj et al., 2020). Toxic metals, classified as non-essential metals, pose severe risks even in minute quantities. Essential and non-essential metals exist in the environment as trace elements but accumulate in specific regions due to human activities like urbanization, industrialization, mining, agriculture, and smelting (Houri et al., 2020). The increased presence of Heavy Metals (HMs) in soil and the environment has garnered significant attention recently due to their widespread distribution, non-degradability, toxicity, accumulation potential, and persistence. Extensive evidence suggests that HMs adversely affect various soil properties, including physical, biological, and chemical characteristics. As a result of their prolonged presence in soil, HMs pose a significant threat to human health by enabling harmful metals to enter the food chain (Mao et al., 2019; Mitra et al., 2022). The widespread destruction of existing vegetation and the establishment of new vegetation exacerbate the adverse effects of HMs on soil surface, structure, fertility, nutrient cycles, and microbial communities. HMs indirectly impact soil enzymatic activities by altering soil microbial communities’ size, composition, and activity (Ding et al., 2022). These chemicals interfere with essential metabolic functions like respiration, denitrification, and enzyme activity, leading to a reduction in the abundance of certain microbial populations. Furthermore, HMs negatively affect the development of cell membranes, hindering microbial cell division, transcription, and protein denaturation (Sobolev and Begonia, 2008; ). The composition of soil, encompassing factors such as texture, clay content, organic matter, pH, as well as the presence of inorganic anions, cations, and metal speciation, all play significant roles in shaping the impact of metals on soil biology. Similarly, heavy metal (HM) contamination significantly affects soil quality, fertility, plant health, and yield. HM contamination disrupts crucial biological processes including seed germination, water regulation, photosynthesis, electron transport, stomatal conductance, CO2 assimilation, antioxidant defense mechanisms, solute balance, mineral uptake, and overall plant growth. Such disruptions can ultimately lead to plant mortality (; Kalaivanan and Ganeshamurthy, 2016; Riyazuddin et al., 2022). Furthermore, HM toxicity impedes plant development and metabolism by causing oxidative damage to cellular structures and interfering with cytoplasmic enzymes (Kalaivanan and Ganeshamurthy, 2016). Reduced yields resulting from impaired plant growth contribute to escalating food insecurity. The extensive presence of HMs in soil poses risks to human health as these contaminants can leach into other environmental compartments such as groundwater, rivers, and crops (). Water exceeding allowable HM concentrations loses its quality, rendering it unsuitable for drinking and irrigation (Tan et al., 2016). HMs can enter the human body through various routes including ingestion, skin contact, food consumption, and water intake. Prolonged exposure to certain metals can have detrimental health effects, which may not manifest until years after exposure begins. The duration and intensity of exposure are critical determinants of toxicity levels (Jia et al., 2018; Mao et al., 2019; ; Sall et al., 2020; Ding et al., 2022).

Persistent Organic Pollutants (POPs) are synthetic chemicals that endure in the environment, accumulate in organisms, and pose potential risks to human health and ecosystems (; Tufail et al., 2022). Primarily human-made, these substances can traverse vast distances via air and water, impacting remote regions. The escalating apprehension over POPs’ adverse impacts on human and plant health is evident (refer to Table 3), underscoring the global challenge of controlling and managing these pollutants.

TABLE 3

SubstanceEffects on human healthEffects on plantsCommon sourcesReferences
Heavy Metals
Lead (Pb)- Neurological damage, developmental delays in children- Inhibits photosynthesis, damages cell membranes- Lead-based paints, contaminated soil, waterLi et al. (2022), Nawaz et al. (2021), Yu et al. (2022)
Cadmium (Cd)- Kidney damage, bone disorders, lung cancer- Inhibits root growth, disrupts mineral uptake- Industrial emissions, phosphate fertilizersLi et al. (2022), Nawaz et al. (2021), Yu et al. (2022)
Mercury (Hg)- Neurological damage, birth defects, cardiovascular issues- Inhibits chlorophyll synthesis, damages cell structure- Coal combustion, mining, seafood contaminationRiseh et al. (2022), Verma and Sharma (2017), Wang, Wang, et al. (2023), Yang et al. (2023)
Arsenic (As)- Skin lesions, cancer, cardiovascular diseases- Inhibits growth, disrupts enzyme functions- Natural occurrence, mining, agricultural pesticides, , Eyankware and Obasi (2021)
Chromium (Cr)- Respiratory issues, cancer, liver damage- Inhibits seed germination, disrupts root growth- Industrial discharges, leather tanning, mining, , Eyankware and Obasi (2021)
Nickel (Ni)- Skin allergies, lung cancer, kidney damage- Inhibits enzyme activity, disrupts nutrient uptake- Stainless steel production, batteries, metal platingWu et al. (2021), Xia et al. (2018)
Barium (Ba)Renal and cardiac dysfunction, respiratory failure, pulmonary paralysis, and internal bleeding- Photosynthesis inhibition- Petroleum industry, medicinal applications, semiconductors production, steel industryDell'Anno et al. (2023), Ma et al. (2018)
Copper (Cu)Increased levels cause liver cirrhosis and persistent anaemia in addition to the typical side effects of nausea, vomiting, and abdominal pain- Negative effects on development and metabolic abnormalities- Ore mining, bio-solids, fertilizers and pesticide manufacturing, smeltingLin et al. (2003), Shabbir et al. (2020), Wu et al. (2018)
Zinc (Zn)Electrolytic imbalance, nausea, fatigue, tiredness, stomach pains, diarrhea, muscle weakness, dehydration, and kidney failure- Interferes with gene regulation- Emission from tire industry, Food additives, High tension linesWyszkowska et al. (2013)
Persistent Organic Pollutants (POPs)
Polychlorinated Biphenyls (PCBs)- Cancer, reproductive issues, immune system disorders- Inhibits photosynthesis, damages cell membranes- Electrical equipment, insulation materialsGrimm et al. (2020), Xiang et al. (2020), Zhou et al. (2023)
Dioxins and Furans- Cancer, hormone disruption, developmental issues- Inhibits growth, disrupts reproductive functions- Waste incineration, industrial processes, herbicidesLanda-faz et al. (2021)
Dichlorodiphenyltrichloroethane (DDT)- Cancer, reproductive issues, developmental delays- Inhibits photosynthesis, damages cell membranes- Agricultural pesticides, insect repellentsRusso et al. (2019), Talukdar et al. (2020)
Polybrominated Diphenyl Ethers (PBDEs)- Neurological damage, hormone disruption, thyroid disorders- Inhibits growth, disrupts reproductive functions- Flame retardants in electronics, furnitureLanda-faz et al. (2021)
Hexachlorobenzene (HCB)- Liver damage, immune system disorders, cancer- Inhibits photosynthesis, damages cell membranes- Pesticides, industrial processes, incinerationHuang C. C. et al. (2021), Huang et al. (2020)
Endosulfan and derivatesHeart diseaseInhibitory effect on plant growthCropsLanda-faz et al. (2021)
MirexMalfunction of endocrine system, decreased body weight, hepatomegaly, induction of mixed function oxidasesDecreased dry biomass, reduced growthChemicals used for ant and mites removalThakur et al. (2023)
ChlorpyrifosCardiac system and central nervous system malfunction and disordersDetrimental to plant growth and productivity.Major chemicals used for eradiating insectsHuang et al. (2022), Shi et al. (2019), Ubaid ur Rahman et al. (2021)
HeptachlorDisorders affecting the gastrointestinal and neurological systems.Affect the shoot and root length of test plantsMajor chemicals used for eradiating insectsThakur et al. (2023), Thakur and Pathania (2019)

A comprehensive overview of the effects of various heavy metals and persistent organic pollutants on both human health and plants, along with their common sources.

POPs infiltrate the human body through consumption of contaminated food, water, and air. They are lipophilic and accumulate in fatty tissues, where they can stay for years, leading to chronic exposure (Devi, 2020). POPs are linked to a wide range of health problems, including cancer, reproductive disorders, immune system dysfunction, neurodevelopmental disorders, and endocrine disruption, as mentioned in Table 3. Exposure to POPs during pregnancy can also have adverse effects on fetal development, leading to congenital disabilities and developmental delays. One of the most well-known and widely studied POPs is polychlorinated biphenyls (PCBs) (; Grimm et al., 2020). These chemicals were previously utilized in various applications, such as electrical equipment, transformers, and hydraulic fluids, until their prohibition in the 1970s. Despite the ban, they persist in the environment, potentially accumulating in the food chain and posing risks to human exposure. PCBs have been associated with a spectrum of health issues, including cancer, immune system dysfunction, and developmental delays. Another category of Persistent Organic Pollutants (POPs) receiving recent attention is per- and polyfluoroalkyl substances (PFAs) (Wang et al., 2023). These compounds are used in various products, including non-stick cookware, water-resistant clothing, and firefighting foam. PFAs exhibit high persistence in the environment and can accumulate in the human body, leading to adverse health effects similar to PCBs, including cancer, immune system dysfunction, and developmental delays (Saibu et al., 2023). Dioxins and furans, also categorized as POPs, are byproducts of industrial processes like waste incineration and paper bleaching. Exposure to these chemicals can result in adverse health effects, such as cancer, reproductive disorders, and immune system dysfunction.

Additionally, children exposed to dioxins and furans may experience developmental delays and cognitive impairment. In response to growing concerns regarding the detrimental impacts of POPs, the international community has initiated measures to control and manage these chemicals. The Stockholm Convention on Persistent Organic Pollutants, enforced in 2004, aims to eliminate or restrict the production and usage of POPs. Currently, the convention identifies 28 chemicals as POPs, including PCBs, dioxins, and furans (Yanitch et al., 2020; Saibu et al., 2023; Zhou et al., 2023).

3 Exploring the rhizosphere: importance and significance

The rhizosphere soil region is nutrient-rich, where plant roots stimulate chemical and biological processes (). The plant and many macro- and microorganisms interact uniquely in the rhizosphere, such as viruses, bacteria, fungi, protozoa, algae, nematodes, and microarthropods. These interactions contribute to the plant’s overall development (; ; Pathania et al., 2020; ). Rhizospheric microorganisms that help plant growth can regulate plant development and yield. Rhizobacteria play a crucial role in the rhizosphere’s functioning and significantly impact plant physiology and growth (). Three distinct zones make up the rhizosphere (McGrath et al., 2001), The rhizosphere, the small zone of soil surrounding plant roots, is a dynamic environment characterized by intricate interactions between plants and microorganisms. Understanding the relevance of each rhizospheric zone is critical for comprehending the functions of microbial activity and plant interaction (). The rhizosphere is divided into three zones: the endorhizosphere, the rhizoplane, and the ectorhizosphere. Each zone has a specific role in microbial activity and plant contact.

3.1 Endorhizosphere

The endorhizosphere refers to the plant root’s interior tissues, including the cortex and vascular system. This zone is crucial for several reasons:

  • - Microbial Colonization: Beneficial microorganisms, such as endophytic bacteria and fungi, inhabit the endorhizosphere, providing improved nutrient uptake and growth promotion without harming the plant ().

  • - Nutrient Exchange: Close proximity to the plant’s vascular system allows microbes to efficiently exchange nutrients, such as nitrogen from endophytic nitrogen-fixing bacteria.

  • - Disease Resistance: Endophytic microorganisms help resist diseases by producing antimicrobial compounds or inducing systemic resistance ().

3.2 Rhizoplane

The rhizoplane is the root surface where plant roots interact with the soil environment. This zone is significant for:

  • - Microbial Adhesion: Microorganisms, including bacteria, fungi, and archaea, attach to the root surface, often facilitated by root exudates (McGrath et al., 2001).

  • - Nutrient Utilization: Rhizoplane microbes utilize root exudates, which contain nutrients like sugars, amino acids, and organic acids, for their development and activity ().

  • - Biofilm Formation: Microbes on the rhizoplane often form biofilms, enhancing microbial viability, nutrient exchange, and defense against environmental stressors.

3.3 Ectorhizosphere

The ectorhizosphere is the outer zone of soil surrounding the root, influenced by root exudates but excluding the root surface itself. It plays a crucial role in:

  • - Microbial Diversity: This zone supports a diverse microbial community, including free-living bacteria, fungi, protozoa, and nematodes, often with greater diversity than bulk soil (Zhou et al., 2023).

  • - Nutrient Cycling: Ectorhizosphere microbes contribute to nutrient cycling processes like nitrogen fixation, phosphorus solubilization, and organic matter decomposition, enhancing nutrient availability for plants (Pathania et al., 2020).

  • - Plant-Microbe Interactions: Beneficial microorganisms, such as mycorrhizal fungi and rhizobia, form symbiotic relationships with plant roots, promoting nutrient uptake and plant growth.

  • - Soil Structure: Microbial activity in the ectorhizosphere improves soil aggregation and structure, enhancing soil porosity and water retention.

Understanding each rhizospheric zone’s importance is crucial for optimizing agricultural practices and promoting sustainable farming. By managing rhizospheric microbial communities through strategies like crop rotation, cover cropping, and using biofertilizers and biopesticides, farmers can enhance plant health, improve nutrient uptake, and reduce reliance on chemical inputs. Additionally, insights into rhizospheric interactions can guide ecological restoration and natural ecosystem management, contributing to biodiversity conservation and soil health.

3.4 Plant growth-promoting rhizobacteria: key players in plant development and soil fertility

Rhizobacteria that promote plant development in addition to the plant’s natural defense mechanisms are referred to as plant growth-promoting rhizobacteria (PGPRs). Plant-PGPR interaction is crucial to plant development and soil fertility in the rhizosphere (

;

Manoj et al., 2020

;

Zafar-ul-Hye et al., 2020

;

Shabaan et al., 2021

). PGPRs are a class of rhizospheric bacteria that affect plant development and yield in economically important crops.

Streptomyces

,

Serratia

,

Xanthomonas

,

Pseudomonas

,

Enterobacter

,

Klebsiella

,

Bacillus

,

Burkholderia

,

Azospirillum

,

Azotobacter

, and

Arthrobacter

are a few of the genera found in PGPRs (

;

Gururani et al., 2013

). The following is an overview of the roles performed by PGPRs (

;

;

Gulzar and Mazumder, 2022

;

Kuan et al., 2016

;

Sapre et al., 2021

;

Shabaan et al., 2021

;

Thokchom et al., 2017

;

Ullah and Bano, 2015

):

  • 1. The process of plant nutrient uptake

  • 2. Plant development through the synthesis and production of amino acids and other compounds that stimulate plant development

  • 3. Improved microorganisms required for plant development

  • 4. Phytohormone production (auxins, gibberellins, and cytokinins)

  • 5. Nutrient solubilization (Zn, PO4, Fe2+, and Fe3+)

  • 6. Reduced metal toxicity

  • 7. Stimulating metabolic processes in roots using bacteria's other process, i.e., biological nitrogen fixing

  • 8. Enhanced plant disease resistance

Despite their small size, bacteria are the most prevalent organism in the rhizosphere. Pseudomonas, a Gram-negative bacterium genus, is a particularly efficient root colonizer with 108–1012 bacterial cells per gram of rhizosphere soil. In addition to their usefulness as bio-fertilizers, bioenergy generation, and bioremediation (Table 4), PGPRs are efficient plant root colonizers because of the abovementioned characteristics. The primary reason for the efficient colonization of plant roots by PGPRs is their motility and chemotaxis, which contribute to their positive effects ().

TABLE 4

MechanismDescriptionExample PGPR Genera
Biodegradation of PollutantsPGPR can directly degrade organic contaminants like petroleum hydrocarbons, pesticides, and explosives. They break down complex molecules into simpler forms for easier utilization.Pseudomonas, Rhodococcus, Burkholderia
Enhanced Plant Uptake and Metabolism of PollutantsPGPR can stimulate plant growth, leading to increased root surface area and pollutant absorption. They may also facilitate the breakdown of pollutants within the plant tissues.Azospirillum, Rhizobium, Enterobacter
RhizodegradationPGPR secrete enzymes that degrade pollutants within the rhizosphere (root zone). This localized degradation prevents wider contamination and promotes the breakdown of complex molecules.Serratia, Bacillus, Alcaligenes
BioimmobilizationPGPR accumulate and immobilize pollutants within their cells, preventing them from spreading further. This reduces the bioavailability of contaminants and their harmful effects.Pseudomonas, Arthrobacter, Ochrobactrum
BiovolatilizationCertain PGPR can convert pollutants into volatile forms, allowing them to evaporate and disperse harmlessly into the atmosphere. This can be effective for some organic contaminants.Pseudomonas, Bacillus, Variovorax
PhytostimulationPGPR promote plant growth and root development, which enhances the overall soil health and microbial activity. This improved soil microbiome fosters biodegradation of various pollutants.Azospirillum, Arthrobacter, Bacillus
Biocontrol of PathogensPGPR can compete with and suppress soilborne plant pathogens. This reduces competition for resources and protects plant health, indirectly aiding bioremediation efforts.Pseudomonas, Bacillus, Actinomycetes

Plant Growth-Promoting Rhizobacteria (PGPR) and their mechanisms in bioremediation (; Gururani et al., 2013; ; ; Gulzar and Mazumder, 2022; Kuan et al., 2016; Sapre et al., 2021; Shabaan et al., 2021; Thokchom et al., 2017; Ullah and Bano, 2015).

Nitrogen (N) is a critical nutrient in agricultural production, playing a pivotal role in crop yield, particularly for grains such as rice, maize, potatoes, and wheat (Kuan et al., 2016; Rizvi and Khan, 2018). The application of nitrogen fertilizers significantly enhances the productivity of these crops. However, nitrogen utilization efficiency is often compromised due to ammonia volatilization, nitrogen leaching, and denitrification (Kumar and Saxena, 2019). Biological nitrogen fixation (BNF) presents a viable alternative to reduce chemical fertilizers applications. BNF responsible for the majority of Earth’s fixed nitrogen (∼60%). Given the increasing global food demand, optimizing BNF in agriculture is essential (Wickramasinghe et al., 2021). The nitrogen-fixing bacteria Kosakonia radicincitans was isolated from Pennisetum giganteum by Jia et al. (2020). They demonstrated that by combining this bacterium with chemical fertilisers, the total amount of fertiliser needed could be lowered by 25%. This integration significantly improved several plant characteristics, including alkali hydrolyzed nitrogen content, vitamin C and soluble protein amount, chlorophyll amount, soluble sugar amount, and available phosphorus amount. Similarly, Song et al. (2021) conducted a 2-year study assessing the replacement of urea with the cyanobacterium Anabaena azotica in rice cultivation. The investigation determined that using cyanobacteria in place of half of the urea had no negative effect on rice production.

Phosphorus (P) is another crucial macronutrient for plant growth and metabolic processes (Khan et al., 2009). Metal cations like calcium, iron, and aluminium quickly immobilise phosphorus in soils or bind it to mineral surfaces, reducing the amount of phosphorus that plants may access. Phosphates play vital roles in legume biological nitrogen fixation, crop maturation, flower and seed production, root and stem development, photosynthesis, and plant disease resistance (Nath et al., 2017; Wan et al., 2020). Therefore, phosphates are indispensable for agricultural productivity. In their 2020 study, Wan et al. tested eight different bacterial taxa for their ability to solubilize phosphorus. They found that Acinetobacter was the most effective, leading to improved soil fertility and quality. In addition, Liu et al. (2020) showed that specific bacteria release organic acids with low molecular weight, which dissolve inorganic phosphorus, alter soil characteristics, and indirectly affect the microbes in the rhizosphere. Iron, in its most common forms as Fe3+ and Fe2+, is a mineral that plants cannot function without (). Plants are unable to absorb iron from soils because the element is typically present in insoluble forms such hydroxides and oxyhydroxides, especially under aerobic circumstances. Iron is insoluble in water, but bacteria in the rhizosphere manufacture siderophores—small molecules with a strong affinity for iron—those plants can use (Da Silva et al., 2023). Rhizobium, Enterobacter, Pseudomonas, Azotobacter, Bacillus, and Azotobacter are among the plant growth-promoting rhizobacteria (PGPR) that create siderophores (Din et al., 2019). In situations where there is a shortage of iron, these molecules—which are present both within and outside of cells—help dissolve organic compounds and minerals containing iron. They can also form stable complexes with heavy metals and radioactive particles (Din et al., 2019). Soil heavy metal contamination can be reduced and plant growth can be enhanced by PGPR strains that produce siderophore. Phytohormones including gibberellin, cytokinin, and indole-3-acetic acid (IAA) are produced by plant growth-promoting bacteria (PGPB), which impact the hormone balance in plants (Chen et al., 2017). The amount of auxin available to the plant and its sensitivity to the hormone determine how IAA influences root growth. While low concentrations of bacterial auxin stimulate growth, high concentrations of auxin from PGPB, when added to the ideal levels of auxin found in nature, can stunt plant development (Sukul et al., 2021). By encouraging the development of adventitious and lateral roots and boosting the secretion of root exudates, bacterial IAA improves nitrogen absorption. Pseudomonas sp. isolated from soil near Vigna radiata (L.) produced growth-regulating compounds such IAA, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, and siderophores, according to investigation of pesticide-resistant plant growth-promoting rhizobacteria strains. Even when exposed to increasingly high quantities of metalaxyl, carbendazim, and tebuconazole, the PGR-11 strain persisted in producing PGP compounds. High pesticide concentrations have a negative effect on plant development and physiological and biochemical features, according to tests conducted on V. radiata (L.).

3.5 Relationship between heavy metals and the microbiome

Bioremediation technology currently focuses on the interactions between metals and microbes, which can be explained differently. The presence of soil microorganisms in different soil regions is crucial in deciding the fate of heavy metals in the soil (; Gulzar and Mazumder, 2022). These microorganisms are not evenly spread throughout the soil, and heavy metals can severely impact their cellular, biochemical, and molecular processes, putting their survival at risk. Although heavy metals generally have an inhibitory effect at high concentrations, some heavy metals, such as Cadmium, can harm soil microbiota even at low concentrations (Sengupta et al., 2021). Heavy metals are toxic because they inhibit cell growth and development by directly destroying or deactivating critical cellular components, among other things. For example, HMs can cause oxidative stress by ROS production (Husain et al., 2022), disrupting the structure () and function of several active biomolecules like DNA, RNA, and proteins (Gulzar and Mazumder, 2022). For instance, metals like cadmium, mercury, and lead disrupt the ionic balance, harm cell membranes, and even denature proteins (Sobolev and Begonia, 2008; ). In addition to causing ionic imbalance and enzyme inhibition in bacterial systems, copper, nickel, and zinc toxicity has been documented (Ding et al., 2022). Metal ions can block the activity of many enzymes, including superoxide dismutase, catalase, and ascorbate peroxidase (Mitra et al., 2022). In a similar vein, arsenic damages DNA, while mercury impedes the transcription process ().

It has been suggested that microorganisms residing in metal-contaminated soil can transform toxic metals into less harmful molecules. The microbiome can dissolve or solubilize heavy metals, and transition metals can undergo oxidation or reduction without impacting the microbiome’s ability to promote plant growth (Hlihor et al., 2022). In addition, the soil microbiome replenishes the environment by binding, volatilizing, oxidizing, immobilizing, and converting harmful metals into less harmful forms. Consequently, the soil microbiome can remove, restore, precipitate, and detoxify metals by modifying their environmental characteristics and solubility (). These ecological interactions between the microbiota and toxic metals are essential for regulating mobility and decontaminating polluted environments. Nevertheless, the effectiveness of microbial activities depends on various factors, including metal concentration and species, the composition and function of microbiomes, and the environmental state (Kim et al., 2020; Liu et al., 2019).

4 Remediation approach used for HMs and POPs

Understanding chemical characteristics and eliminating heavy metals and pollutants (POPs) from the soil requires efficient solutions. Several strategies have been tried to reduce the harmful effects of POPs, the most prevalent of which involves concentrating on HMs and PAHs found in soil and water, respectively (Tufail et al., 2022). Depending on whether the remediation is conducted on-site (in-situ) or away from the contaminated area (ex-situ), soil and water remediation techniques can be categorized as chemical (using chemicals), physical (using physical agents), or biological (using living organisms) (Cepoi et al., 2022; Kumar et al., 2022; Li et al., 2020). To alleviate POPs, modern techniques have been developed that incorporate the compounds’ molecular size, water solubility, polarity, and volatility, increasing extraction efficiency (Sun et al., 2017). Table 5 presents a compilation of methods utilized for HMs and POPs remediation from the environment, showcasing a summary of different approaches.

TABLE 5

Remediation strategiesMethods adoptedMetals removedDescriptionLimitationsBenefitsReferences
Physical processesFroth floatationCu, Pb, Zn, AsUses air bubbles in soil slurry to extract metal-bearing granules from the soil medium by exploiting hydrophobic variationExpensiveHigh Removal efficiencyPark and Son (2017)
Electrokinetic remediationAs, Cu, PbApplying electrical current to the electrolytic tank de-stresses contaminated soilDepth and soil heterogeneity limitFast, low-energy recoveryKim et al. (2013)
VitrificationCrThe contaminated soils are heated to melting point in order to stabilise themComplicated, expensive, and damaging to soils with high organic matter, dampness, and volatile or flammable organicsIt’s quick, it works for a long time, and it can be used in various different situations
Thermal treatmentHg, Zn, CuHeating polluted soils removes volatile contaminantsCauses potential damage to soil structure, necessitating costly capital expenditures and strict regulation of gas emissionsRapid, risk-free, and producing negligible amounts of secondary pollutantsSong et al. (2017), Wang et al. (2018)
Soil replacementHg, Cd, Ni, Cu, Cr, Pb, Zn, As, Sb, Ba, BeSoil that has been contaminated is either totally or partially replenished with clean soilExpensive, useful only in a restricted areaFor heavily contaminated soilDerakhshan et al. (2018), Valentim dos Santos et al. (2016)
Magnetic separationAs, Cu, Hg, PbUse the magnetic differences between particles to sort themcostly, has the potential to destroy physical and chemical propertiesSuitable for both small and large particles; exceptionally productive, simple, fast
Hydrodynamic separationAs, Cu, Hg, PbUse centrifugal force and particle settling velocities in water flowsThe process is expensive, and it might change the soil’s qualities (texture and particle size), resulting in less fertile soilEconomical, simple, and fast, appropriate for many sands
Chemical processesStabilizationCd, Pb, Zn, As, CrReduces soil metal mobility and bio-availabilityInduces a shift in the soil’s physical characteristicsGood effectiveness, simple, fast, reasonably affordableUllah et al. (2020), Epelde et al. (2014)
Treatment with nanoparticlesMetals and metalloidsActivated by the NP-specific surface area, this process includes co-precipitation, precipitation, redox reactions, and adsorptionControversial because the effects of NP on soil composition, biodiversity, and NP-plant interactions are unknown and may constitute a long-term harmRapid, preciseSun et al. (2020)
Electrochemical remediationCd, Co, Cr, Cu, Pb, ZnIncludes the processes of electrolysis, electrophoresis, electro-osmosis, and electromigrationExtensively difficult to implementeffective even in soils with low permeability, and it does not cause substantial alterations to the soil’s attributesXu et al. (2019), Yang X. et al. (2020)
Soil washingPb, Cd, Zn, CuMetals in contaminated soils can be leached with the help of reagents and extractantsCostly damage to soil structure and nutrient levelsMetals are eliminated permanently; the process is user-friendly and quickFeng et al. (2020), Wang et al. (2020)
Stabilization/solidificationPb, ZnWaste is enclosed in a monolithic solid of high integrityTime-consumingEfficient, straightforward, fastLiu et al. (2015)
Biological processesBiobleachingAny metalsSubstances produced by microorganisms are capable of dissolving metalsSlower, environment-sensitive bacteria cannot bind to cell surfactantsaffordable and low impact on the environmentYang X. et al. (2020)
BiosorptionAll forms of metalsMetals are attached to the membranes of both living and nonliving cellsInfluenced by nutrition and atmosphereQuick, risk-free, and cheap as well as very efficientRizvi and Saghir Khan (2019), Rizvi et al. (2020), Saleem et al. (2022)
Microbial remediationAll types of metalsInoculating soil/seeds/roots with metal-tolerant plant beneficial microorganismsThe process is slow, and environmental influences may affect itAffordable, environmentally friendly, and not generating secondary pollutantsRizvi and Khan (2018), Rizvi et al. (2020), Saleem et al. (2022)
Microbes with plantsAlmost all metalsMetal-tolerant bacteria boost plant development when seededCompetition from natural microflora, environmental variablesEffective, inexpensive, environmentally friendly, and a source of vital nutrients for plant growthKhan et al. (2009)
PhytoremediationCr, Zn, As, Cd, Pb, As, Zn, Pb, CdHigh-biomass plants are usedLong durationEconomical, low-impact on the environment, and time-savingSigua et al. (2019), Yang et al. (2017)

Techniques for the physical, chemical, and biological remediation of metals at both laboratory and field scales.

4.1 Physicochemical approaches utilized for remediation

Ultrafiltration, solvent extraction, osmosis, nanofiltration, incineration, flotation, ion exchange, electrodialysis, fixation (i.e., nitrogen), conventional and advanced oxidation, coagulation, and precipitation are some of the physicochemical processes that have been used to get rid of HMs and POPs (Kadam et al., 2019). As a physicochemical technique, adsorption has great promise for eliminating HMs and POPs from the environment. Adsorption is widely used in industry because of its remarkable potential efficiency, low energy requirements, molecular level preference, malleability, and capacity to separate various chemical substances (Priyadarshanee and Das, 2021).

Another standard method of water purification is electro-coagulation (; Titchou et al., 2021). Research studies () have shown the application of iron electro-coagulation to remove As (III) from the environment. After being subjected to microfiltration, the concentration of additional HMs (Cr, Pb, and Ni) in oily water dropped to 10 mg/L from 35 mg/L (Changmai et al., 2019). Commercial electro-coagulation systems maintain a steady current of 5–20 mA/cm2 for optimal effluent removal. Advanced oxidation processes (AOPs) and conventional oxidation processes (COPs) are two types of chemical treatments (Silvianti et al., 2020). Photocatalysis processes, solar-Fenton, electron-Fenton, and Ferrate ion, all AOPs, have greatly facilitated the remediation process of HMs (Mazumder et al., 2020). Nevertheless, ozonization, hydrogen peroxide (H2O2), chlorination, and photolysis are used in COPs to clean water, and their application will produce byproducts and radicals. Fruit waste, such as banana peel, egg shells, coconut husks, and nutshells, as well as tannin-rich materials like rice husk and fertilizer wastes, are all examples of bioadsorbents to treat water and soil (O’Connell et al., 2008; Zhao et al., 2018). Furthermore, several soil-derived adsorbents, such as fly ash and red mud (Dash et al., 2018), zeolites and clays (Titchou et al., 2021), new carbon nanomaterials (NMs), and metal oxides, showed improved removal effectiveness when tested on a variety of contaminants and HMs (Chakraborty et al., 2022).

4.2 Biological approaches utilized for remediation

Microbial bioreactors (MBRs) have been shown to effectively decontaminate wastewater using a combinatorial approach of microbial biodegradation and physical retention at the membrane surface (Tufail et al., 2022; Zhang et al., 2020). However, Membrane fouling makes it challenging to eliminate specific POPs. As a result, a hybrid technique involving an electrochemical MBR has been developed to remove nearly all toxins at a fixed electric potential from wastewater (Hube et al., 2020). Compared to controlled MBR, this approach is three times more reliable and may be used for three times as long. The build-up of pesticides, PAHs, and HMs in natural resources is a topic of discussion on a global scale. Pollutants remained in the soil for a long and leaked into the ground and surface water. In order to produce sustainable habitats, it is crucial to break down harmful chemicals in the soil (Russo et al., 2019; Rigoletto et al., 2020; Saha et al., 2021). Bioremediation is superior to the conventional physicochemical approach of removing pollutants from soil and water. Microbe-mediated biodegradation of HMs and organic pollutants is emerging as a modest but feasible answer to all these problems, often known as bioremediation (Tyagi and Kumar, 2020; Sreedevi et al., 2022; Tufail et al., 2022; Liaqat et al., 2023; Masotti et al., 2023; Saibu et al., 2023). Compared to chemical and physical approaches, this technology is more cost-effective, less invasive, environmentally benign, and long-lasting.

4.2.1 Bacterial-mediated bioremediation

Bacteria might adapt or be resistant to metal toxicity using various approaches, i.e., synthesis of metallothioneins, active transport or efflux mechanisms, morphological changes, synthesis of siderophores, biotransformation of toxic metals, and synthesis of exopolymeric compounds (Funtikova et al., 2023; Liaqat et al., 2023; Sevak et al., 2023; Wang et al., 2023; Zhou et al., 2023). Figure 1 presents the few microbial approaches used for HM remediation from the soil.

FIGURE 1

Bacteria are well-known for their ability to degrade or mineralize pollutants through enzyme-catalyzed catabolic action (Tables 6, 7). Numerous catabolic genes that rely on PAHs and are remarkably conserved have been identified during bioremediation studies (; ). These genes are present in gram-positive bacterial species and include phd, pdo, nid, and nar, and in gram-negative bacterial species and include phn, pah, ndo, nah, and nag (Sakshi and Haritash, 2020). Analysis showed that crude oil might be biodegraded by the bacteria Pseudoalteromonas agarivorans, Isoptericola chiayiensis, Rhodococcus soli, and Bacillus algicola in less than 2 weeks (Lee et al., 2018). Most small molecules with carbon atoms between C9 and C14 were entirely decomposed, while those with C15 and C20 were almost completely broken down. The larger-sized molecules, on the other hand, were substantially broken down. Another study reported that after 30 days of remediation, bacterial consortiums obtained from China’s Yangtze River Delta broke down 44.5% of total petroleum hydrocarbon (TPH) (Jia et al., 2018). Chlorpyrifos (CPF) breakdown was studied in two different bacterial species Bacteroides megaterium CM-Z19 and Pseudomonas syringae CM-Z6. Five days of incubation at 37°C resulted in a 92.6% and 99.1% degradation of chlorpyrifos-methyl-Z19 and chlorpyrifos-methyl-Z6, respectively, at an initial 100 mg/L concentration (Zhu et al., 2019). Nevertheless, 200 μg per liter of CPF can be degraded by Cupriavidus nantongensis X1T in about 48 h. C. nantongensis X1T species may survive in temperatures between 30°C and 42°C, and pH ranges between 5 and 9. It has a CPF tolerance of 500 mg/L (Shi et al., 2019). Cupriavidus sp. DT-1 has been shown to successfully degrade CPF in liquid media, mineralizing both CPF entirely after 14 h at pH 7°C and 30°C. In the same settings, 90% of chlorpyrifos in soil media degrades after 30 days (Lu et al., 2013). The most efficient microorganisms, P. putida MAS, can break down 90% of CPF in 24 h (Kamika and Momba, 2013). Recent studies indicate that aerobic bacteria, such as Sphingobium sp. strain BHC-A and Schistosoma japonicum UT26, can fully degrade lindane in an aerobic environment (Perera and Hemamali, 2022). Atrazine-contaminated soil from the Vetiver rhizosphere reported two bacterial species: Paenarthrobacter aurescens TC1 and Arthrobacter MCM B-436. Atrazine degradation in P. aurescens TC1 is controlled by trzN, atzC, and atzB genes. Arthrobacter sp CW-1 breaks down dimethyl phthalate (DMP) in anaerobic environments (Jia et al., 2021). Nicotine degradation in Arthrobacter nicotinovorans is mediated by the plasmid pAO1 (Guo et al., 2019). Rhodococcus pyridinivorans SS2 and Rhodococcus ruber SS1 can effectively remediate triCB and dichlorobiphenyl (diCB) (Xiang et al., 2020). Pseudomonas sp. breaks down - Hexabromocyclododecanes (HBCD) at concentrations as low as 50 mg/L in about 5 days, but at 640 mg/L, it takes 8 days to break down (Huang L. et al., 2021; Huang et al., 2022). Bacillus sp. can break down HBCDs at 320 mg/L in about 4 days (Huang et al., 2022). Pseudomonas aeruginosa HS9 can degrade 69% of 1.7 mg/L HBCDs in 14 days. Table 6 provides a detailed overview of diverse bioremediation strategies utilized by microorganisms to effectively eliminate Heavy Metals (HMs) and Persistent Organic Pollutants (POPs) from contaminated environments.

TABLE 6

MechanismDescriptionExamples of microorganisms
Bioremediation mechanisms of heavy metals (HMs)
BiosorptionMicroorganisms absorb heavy metals onto their cell surfaces or within their biomass.Pseudomonas aeruginosa, Bacillus subtilis, Saccharomyces cerevisiae
BiomineralizationMicroorganisms convert soluble heavy metals into insoluble forms or minerals, reducing their bioavailability.Desulfovibrio desulfuricans, Bacillus sp., Pseudomonas putida
BioaccumulationMicroorganisms accumulate heavy metals within their cells to concentrations higher than those in the surrounding environment.Spirodela polyrhiza (Duckweed), Chlorella vulgaris (Algae), Thlaspi caerulescens (Metal hyperaccumulator plant)
BioreductionMicroorganisms reduce heavy metal ions to less toxic or less mobile forms.Geobacter sulfurreducens, Shewanella oneidensis, Clostridium sp.
Bioremediation Mechanisms of Persistent Organic Pollutants (POPs)
BiodegradationMicroorganisms enzymatically degrade organic pollutants into simpler, less harmful compounds.Pseudomonas putida, Rhodococcus sp., Mycobacterium sp.
PhytoremediationPlants absorb and detoxify organic pollutants from the environment, with associated microorganisms enhancing degradation processes.Populus spp. (Poplar trees) with mycorrhizal fungi, Brassica juncea (Indian mustard) with rhizospheric bacteria, Phragmites australis (Common reed) with mycorrhizal fungi
CometabolismMicroorganisms metabolize pollutants using enzymes produced during the degradation of other compounds.Methylosinus trichosporium, Sphingomonas sp., Mycobacterium vaccae
Anaerobic BiodegradationBiodegradation of organic pollutants under anaerobic conditions, often involving microbial consortia.Dehalococcoides sp., Methanosarcina sp., Desulfitobacterium sp.

A comprehensive breakdown of various bioremediation mechanisms employed by microorganisms for the removal of heavy metals (HMs) and persistent organic pollutants (POPs) (Guo et al., 2019; Huang et al., 2021; Jia et al., 2021; Huang et al., 2022).

TABLE 7

MicroorganismHMsOutcome or resultReferences
Bacillus megateriumPbcytoplasmic accumulationChen et al. (2019)
Bacillus simplexPbMetal accumulation endogenously ranges from 88.5% to 98.5%Chamekh et al. (2021)
Lactic acid bacteriaPbMetal accumulation endogenously up to 99.9%Liu et al. (2019)
Ralstonia metalliduransPbTrivalent-cation efflux systems (chemi-osmotic pumps) used for metal accumulationWang et al. (2023)
Pseudomonas marginalisPblead extracellularly remediatedLiaqat et al. (2023)
Pseudomonas aeruginosa ASU 6aPbBoth dead (123 mg/g) and alive cells (79 mg/g) showed lead accumulationGabr et al. (2008)
Bacillus sp. ATS-2Pb91.73% Pb(II) accumulation intracellular
Bacillus subtilis PbRB3PbBacillus subtilis PbRB3 removed >80% of Pb from culture solution
Staphylococcus aureus and Citrobacter freundiiPbDeposition of lead-phosphate intracellularlySuresh et al. (2021)
Frankia sp.PbPb–PO4 compounds produced from cells deposited Pb2+ with maximum ratesFurnholm et al. (2017)
FrankiaCuFrankia had copper in its cells or on its surfaceLiu et al. (2015)
Acidithiobacillus ferrooxidansCuRegulating phosphate aggregates by stimulating polyphosphate degradation and copper-phosphate complexationZhu et al. (2022)
Bacillus genusCdThe Cd concentration demonstrated a reduction of between 28% and 40%Zhang et al. (2021)
Zhang et al. (2023)
Bacillus mycoides and Micrococcus roseusCdBacterial growth and maize shoot nutrient uptakeMonachese et al. (2012)
Burkholderia dabaoshanensis sp. novCdThe cell surface’s amide, carboxy, and phosphate produce low-molecular-weight (LMW) organic acids to complex or chelate Cd2+ in the adsorptive pathway for cadmiumZhu et al. (2022)
Zhu et al. (2020)
Lactic acid bacteriaCdThe Cd concentration reduced from 69.45% to 79.91%Li et al. (2021)
Acidophilic strain 62BNCdReduction in concentration by 50% within 60 daysRani et al. (2009)
Bacillus licheniformis spCdReduction of Cd up to 24.51 mg/g
Pseudomonas sp.CdIntracellular accumulation of Cd2+ up to 93.5%
Halobacillus sp. KN57NiReduction of Ni up to 111.11 mg/gTorabia and Kardel (2019)
Bacillus thuringiensis and Staphylococcus capitisCrIn 96 h of treatment, >90% reduction of Cr(VI)Suresh et al. (2021)
Pseudomonas putidaZn and CdP-type ATPases and two CBA transportersGentry et al. (2004)
Lu et al. (2017)
Streptococcus thermophilusZn and CdcadCSt and cadASt genes responsible for cadmium/zinc resistanceSchirawski et al. (2002)
Pseudomonas aeruginosaZn, Cd, and HgUp to 99% reduction in HMs concentrationImron et al. (2021)
Enterobacter cloacaePb, Ni, Cd, and CrHeavy metal toxicity headed Cd > Cr > Pb > Ni. Heavy metals decreased P solubilization, pH, and bacterial biofilm growthSyed et al. (2022)
Burkholderia fungorumCd, Pb, and ZnThe accumulation of metals in the cell wall and the interior region of bacterial cell occur. High metal tolerance and catabolic activityYang et al. (2015)
Thiobacillus thiooxidansCu, Zn, and CrReduction in a final concentration of HMs Cu (81.89%), Zn (64.05%), and Cr (71.08%)Nagashetti et al. (2013)
Klebsiella variicolaAs, Cd, and PbRemoval of HMs from polluted soil using genetically engineered Klebsiella variicolaYetunde Mutiat et al. (2018)
Burkholderia sp.Cu, Cd, Mn, and PbHMs-contaminated soil minerals adhere to Burkholderia sp. and produce a biosurfactant-metal complexYang Y.-C. et al. (2020)
Bacillus cereus KMS3-1Pb, Cu, and CdPb(II) (78.74 mg/g), Cu(II) (71.42 mg/g), and Cd(II) (54.05 mg/g) maximum adsorption capacity (Qmax).Mathivanan et al. (2021a), Mathivanan et al. (2021b)

Various bacteria used for remediation of HMs in soil.

Halophilic bacteria possess extremozymes that can operate effectively in severe conditions, which makes them a promising choice for bioremediation applications. These halophilic bacteria produce an extremozyme with unusual properties, including resistance to heat, acidity, organic solvents, and strong ions. Microprecipitation or proton exchange aids in attaching these bacteria to HMs via an extracellular polymeric material (Kaushik et al., 2021). The negative charge on cell surfaces can be attributed to various functional groups, including sulfate, carboxyl, phosphoryl, and amino functional groups. These functional groups possess negatively charged atoms or groups of atoms, such as oxygen or sulfur, which contribute to the overall negative charge of the cell surface (Dawwam et al., 2023; Syed et al., 2022). The negative charge of these functional groups plays an essential role in the interaction of biomass with metal ions. These groups serve as ion exchange sites and can bind metal ions through a process known as cation exchange. During cation exchange, metal ions, such as hydrogen ions, are exchanged for positively charged ions on the biomass surface (Kaushik et al., 2021). Microorganisms employ various mechanisms to eliminate heavy metals from contaminated soils. These include precipitation, biosorption by sequestering them in intracellular metal-binding proteins (metallothioneins), and converting them into harmless forms through an enzymatic transformation, as presented in Figure 2.

FIGURE 2

In addition, the anionic functional groups in the cell walls of gram-positive and gram-negative bacteria have an essential function in binding metals. The negatively charged groups allow the bacteria to bind metal ions on the surface or within the cell wall. Binding metals is vital for bacteria’s survival as metal ions are necessary for many cellular processes, such as enzyme activity and energy metabolism (Pachaiappan et al., 2021). It has been reported that Methanothermobacter thermautotrophicus can convert chromium (VI) to chromium (III) and then immobilize chromium (III) as hydroxide or oxide. Bacillus cereus and Shewanella have been shown to decrease Cr (VI) and its immobilization (Chen et al., 2012) as shown in Figure 2. Table 7 enumerates diverse bacterial species employed in soil for the remediation of heavy metals (HMs), showcasing their effectiveness in mitigating environmental contamination.

4.2.2 Fungi-mediated bioremediation

Fungi are a diverse group of eukaryotic organisms that obtain their nutrients from organic matter in their environment, and they are often referred to as saprophytic organisms. Fungi have been present on Earth for millions of years, and they play essential roles in various ecological processes such as decomposition, nutrient cycling, and symbiosis. They are exceptionally efficient in decomposing PAHs and HMs due to their specificity for excessive refractory chemicals and survival potential in harsh natural habitats, i.e., elevated temperatures and reduced pH (; ; Chen et al., 2022; de Moura Dickel et al., 2022). Moreover, the fungus may digest PAHs and HMs “in situ” by producing extracellular enzymes (Liu et al., 2017), which can be done due to the extensively branched mycelia. Fungi have two main approaches for metal detoxification: biosorption (), which includes adhering metals to the membrane, and bioaccumulation, which includes absorbing metals into the cell and metabolizing them (Soleimani et al., 2010). It has been shown that certain fungi, including Gloeophyllum sepiarium, Penicillium chrysogenum, Aspergillus versicolor, Aspergillus terreus, Aspergillus niger, Aspergillus fumigatus, and Rhizopus oryzae can breakdown PAHs and HMs (Hota et al., 2021). Recently, Chen et al. (2022) evaluated the potential of white rot fungus for the remediation of heavy metal contamination. However, heavy metal concentrations, organic pollutants, and unfavorable environmental conditions can slow this remediation process. Table 8 presents a comprehensive overview of various fungi, algae, and plants utilized for remediating heavy metals (HMs) in soil, emphasizing their mechanisms and target HMs. These organisms play crucial roles in bioremediation by absorbing, accumulating, or transforming HMs through mechanisms such as biosorption, bioaccumulation, and biotransformation. Understanding these biological agents and their specific interactions with HMs is essential for developing effective strategies for soil remediation and environmental protection.

TABLE 8

Organism typeOrganismMechanismsTarget heavy metals (HMs)
Fungi (Mycorrhizal)Glomus intraradices (AMF)* Mycorrhizal symbiosis: Enhances plant metal uptake and tolerance through increased root surface area. * Metal chelation: secretes organic acids that bind and immobilize HMs.As, Cd, Pb, Zn, Cu
Rhizophagus irregularis (AMF)* Mycorrhizal symbiosis. * Metal chelationAs, Cd, Pb, Zn, Cu
Laccaria bicolor (EMF)* Mycorrhizal symbiosis: forms a sheath around plant roots, increasing HM absorption. * Metal chelationAs, Cd, Pb, Zn, Cu
Paxillus involutus (EMF)* Mycorrhizal symbiosis. * Metal chelationAs, Cd, Pb, Zn, Cu
Pisolithus tinctorius (EMF)* Mycorrhizal symbiosis. * Metal chelationAs, Cd, Pb
Fungi (White Rot)Trametes versicolor (Turkey Tail)* Extracellular enzyme production: degrades organic matter, potentially releasing bound HMs. * Metal chelationAs, Cd, Pb, Zn, Cu, Hg
Phanerochaete chrysosporium* Extracellular enzyme production. * Metal chelationAs, Cd, Pb, Zn, Cu, Hg
Pleurotus ostreatus (Oyster mushroom)* Metal chelation. * Bioaccumulation: accumulates HMs within fungal tissues.Cd, Pb, Zn, Cu
Lentinula edodes (Shiitake mushroom)* Metal chelation. * BioaccumulationCd, Pb, Zn
Bjerkandera adusta (Fomes fomentarius - Tinder Bracket)* Extracellular enzyme production. * Metal chelationAs, Pb, Cu
AlgaeChlorella vulgaris* Biosorption: passively binds HMs to their cell walls due to high surface area and functional groups. * BioaccumulationAs, Cd, Cr, Pb, Hg
Scenedesmus sp.* Biosorption * Bioaccumulation. * Metal precipitation: can precipitate HMs as insoluble complexes within or outside cellsAs, Cd, Cr, Pb, Hg
Chlamydomonas reinhardtii* Biosorption * Bioaccumulation. * Metal precipitationAs, Cd, Cr, Pb, Hg
Spirulina platensis* Biosorption. * BioaccumulationAs, Cd, Pb, Hg
Dunaliella salina* Biosorption. * Metal precipitationCd, Pb, Hg
Plants (Hyperaccumulators)Brassica juncea (Indian mustard)* Phytoextraction: Extracts HMs from soil and accumulates them in harvestable plant parts. * Metal chelationPb, Zn, Cd
Salix spp. (Willows)* Phytostabilization: Reduces HM mobility by accumulating and immobilizing them within plant tissues. * Metal chelationAs, Cd
Pteris vittata (Chinese Brake Fern)* Phytoextraction. * Metal chelationAs
Thlaspi caerulescens (Alpine Pennycress)* Phytoextraction. * Metal chelationZn, Cd, Pb
Alyssum murale (Wall Alyssum)* Phytoextraction. * Metal chelationNi, Zn, Pb
Plants (Non-hyperaccumulators)Festuca arundinacea (Tall Fescue)* Phytostabilization. * Metal chelationPb, Zn
Lolium perenne (Ryegrass)* Phytostabilization. * Metal chelationPb, Cd
Agrostis stolonifera (Creeping Bentgrass)* Phytostabilization. * Metal chelationZn, Cu
Salix viminalis (Golden Willow)* Phytostabilization. * Metal chelationCd, Pb
Helianthus annuus (Sunflower)* Phytostabilization. * Metal chelationPb, Cd

A comprehensive details of various fungi, algae, and plants used for remediating heavy metals (HMs) in soil, highlighting their mechanisms and target HMs (Soleimani et al., 2010; ; ; Hota et al., 2021; Chen et al., 2022; de Moura Dickel et al., 2022).

The remediation outcomes appear to be highly sensitive to the types of strains, the types of pollutants, and the reaction conditions. Concentrations of heavy metals or organic pollutants that are too high or too low, or reaction conditions that are too slow or too fast, might impede the cleaning process (Kumar et al., 2023; Palanivel et al., 2023; Tessaro et al., 2023). Zhuo and Fan (2021) have reported an in-depth analysis to evaluate the most current developments in using white rot fungus to degrade organic pollutants. In addition, they deduced that most current bioremediation investigations of white rot fungus are undertaken in controlled laboratory settings. Further research must consider the challenges associated with treating pollution in practice. The white-rot fungus most likely uses laccases, lipases, lignin peroxidase (LiP), manganese peroxidase (MnP), and cytochrome P450 versatile peroxidase to breakdown and decrease PAHs and HMs (El-Khoury et al., 2022; Sanchez-Hernandez et al., 2023; Syed et al., 2014). Lasiodiplodia theobromae, isolated from PAH-polluted soil in Beijing, China, removed 53% of benzo[a]pyrene (BaP) within 10 days of incubation (Punetha et al., 2022). Increasing the incubation period to 2 weeks enhanced the biodegradation potential of Peniophora incarnate strain KUC8836, resulting in the removal of 97.9% of pyrene, 95.3% of phenanthrene, and 95% of fluoranthene, attributed to elevated laccase, LiP, and MnP production (Lee et al., 2014). Within 30 days, Rhizoctonia zeae SOL3, Scopulariopsis brevicaulis, and Pleurotus pulmonarius FO43 achieved near-complete decomposition of pyrene at concentrations of 42%, 64%, and 99%, respectively (; Mao and Guan, 2016). Aspergillus terreus, Trichoderma viride, Trichoderma longibrachiatum, and Aspergillus niger were observed to absorb Pb, Cd, Cr, and Ni at rates of 59.67 mg/g, 16.25 mg/g, 0.55 mg/g, and 0.55 mg/g, respectively (Dell’Anno et al., 2022; Kumar and Dwivedi, 2021). In another study, the highest remediation potentials for Cr (III), Pb (II), Cr (VI), and Cu (II) were found to be 226.6 mg/g, 208.5 mg/g, 207.3 mg/g, and 205.1 mg/g, respectively, when the fungus was immobilized in living form (Hanif et al., 2015). The fungus Aspergillus fumigatus (FS6) and Aspergillus flavus (FS4) eliminated almost 70% of the Cr (VI) from the liquid PDB medium. Cd (II) removal by Aspergillus fumigatus (FS9) was as high as 74% (Talukdar et al., 2020). Sterigmatomyces halophilus, A. restrictus, A. penicillioides, A. gracilis, and A. flavus and all of which are obligate halophilic fungi, showed efficient biosorption for cadmium, copper, ferrous, manganese, zinc, and lead (de Moura Dickel et al., 2022; Hota et al., 2021; Kumar and Singh, 2023; Tessaro et al., 2023). S. halophilus and A. flavus demonstrated the highest adsorption levels, averaging 83%–86%. The fungi Mucor alternans, Phanerochaete chrysosporium, Trichoderma viride, Rhizopus arrhizus FBL 578, Fusarium oxysporum, and Trichoderma hamatum FBL 587 are long-established as DDT degraders (Russo et al., 2019). When endosulfan is exposed to Trichoderma harzianum, it is oxidized to endosulfan sulfate and then degraded naturally (Landa-faz et al., 2021). In PAH-contaminated industrial soil, the fungus Irpex lacteus and Pleurotus ostreatus can break down the PAHs. In 5 days at 26.8°C and pH 6.5, Cladosporium cladosporioides degrades 50 mg/L CPF ().

4.2.3 Microalgal-mediated bioremediation

Algae offers various advantages as a decontaminating agent, including low cost, easy handling, non-pollution, quick metal contamination removal for recovery, and no additional wastage. Microalgae exhibit the capability of bio-remediating environmental-contaminants (ECs) through three distinct approaches: bio-uptake, bio-adsorption, and bio-degradation (Table 8) (Goswami et al., 2022; Kashem et al., 2023; Tambat et al., 2023). Bio-adsorption is the process by which contaminants are adsorbed onto the surface of the microalgae cells without any cellular uptake or degradation. This process depends on the physicochemical properties of both the contaminant and the microalgae cells, and it can be affected by factors such as pH, temperature, salinity, and ionic strength (Goswami et al., 2022). Bio-adsorption can be an effective method for removing low concentrations of contaminants from the environment, but it is not a long-term solution, as the contaminants can be released back into the environment over time (Dubey et al., 2023). Bio-uptake is the process by which contaminants are taken into the microalgae cells and accumulated within the cells (Dubey et al., 2023). This process can occur through passive diffusion or active transport, depending on the contaminant’s physicochemical properties and the cellular membrane. Bio-uptake can be an effective method for removing moderate to high concentrations of contaminants from the environment, as the contaminants are sequestered within the cells and are not released back into the environment. Bio-degradation is the process of metabolizing contaminants and breaking them down by the microalgae cells into less toxic or non-toxic compounds (; Goswami et al., 2022). This process depends on the microalgae cells’ metabolic pathways and the contaminants’ nature. Bio-degradation can effectively remove complex or persistent contaminants from the environment, but it requires specific conditions and nutrients to support the growth and metabolism of the microalgae cells. Bio-adsorption occurs when environmental contaminants (ECs) link to organic substances released by cells or components of the cell wall (Das et al., 2022; Satya et al., 2023). Alternatively, bio-uptake occurs when pollutants bind to intracellular proteins and other substances and involve the subsequent intracellular transit through active transport, assisted diffusion, or simple diffusion. Microalgae use a catalytic metabolic process to break down the chemicals into their parts to biodegrade ECs. Bio-degradation is an essential approach for cleaning up hazardous toxins, which works more like a bioreactor than a biofilter by breaking down the contamination into less dangerous chemicals (Sher and Rehman, 2019; Leon-Vaz et al., 2021; Chebotaryova et al., 2023). It could take place inside cells, outside cells, or in a hybrid form. Spirulina, Scenedesmus, Phormidium, Oscillatoria, Nodularia, Desmodesmus, Cyanothece, Chlorella, Botryococcus, and Arthrospira are a few of the microalgal genera used in bioremediation (Dwivedi, 2012; Dubey et al., 2023). Chlorella vulgaris is effective at degrading acenaphthene and fluoranthene, according to research by Touliabah et al. (2022). The microbes Lyngbya digueti, Phormidium mucicola, Oscillatoria princeps, Anabaena variabilis, and Westiellopsis prolific were helpful in the reduction of quantity of various petroleum hydrocarbons in oil refinery effluent, which ranged from 24% to 92% reduction (Takáčová et al., 2014). It was reported that Chlorella kessleri could degrade 3,4-benzpyrene (29%) when exposed to light at a strength of 13.5 W per square meter. Similarly, Chlamydomonas reinhardtii was reported to decompose benz(a)anthracene at a rate of 10 mg/L in 11 days (Luo et al., 2020; Luo et al., 2020). The breakdown of homogentisate resulted in a rise of gene expression that encodes for ubiquinol oxidase, carboxy-methylene-butenolide, carboxylase/oxygenase (Rubisco), ribulose 1,5-bisphosphate, and homogentisate 1,2-dioxygenase (HGD) enzymes. Chlorella vulgaris biomass is an effective biosorbent for the removal of copper (Cu2+), Cadmium (Cd2+), and lead (Pb2+) from a mixed solution containing 50 mg dm3 of each metal ion (Goher et al., 2016). After being treated with Spirulina sp, Ca2+ was reduced by 98% and Cu2+ by 91% in municipal wastewater. Another study (Yang et al., 2015) found that Chlorella minutissima could remove 84% of Cu2+, 84% of Mn2+, 74% of Cd2+, and 62% of Zn2+ from municipal garbage. Microalgal biochar has been shown to remove Cr (VI) from water with 100 percent efficiency by Daneshvar et al. (2019), while Cheng et al. (2017) have studied the biosorption and kinetics of Cd (II) removal using both live and dead C. vulgaris. The research findings indicate that both viable and decaying cells of C. vulgaris exhibit a notable ability for adsorbing Cd, demonstrating efficiencies of 95.2% and 96.8% respectively.

4.2.4 Plant-mediated bioremediation

Plants are used in phytoremediation, a form of bioremediation, to clean up polluted environments such as soil, water, and air. Methods include phytotransformation, phytostabilization, rhizofiltration, phytostimulation, rhizodegradation, phytodegradation, phytovolatilization, and phytoextraction are all part of the broader field of phytoremediation (Nedjimi, 2021; Shabaan et al., 2021; Oladoye et al., 2022) as shown in Figure 3 and Table 8.

FIGURE 3

Many plant species can absorb, bioaccumulate, immobilize, and degrade environmental pollutants. Some plants that can be utilized for HMs and POPs phytoremediation of soil include Cucurbita pepo, Zea mays, Nicotiana tabacum, Medicago sativa, Alyssum murale, Achillea millefolium, Aeolanthus biformifolius, Arabis gemmifera, Phytolacca americana, and Pteris vittata (Kurniawan et al., 2022; Li et al., 2023; Rahman and Singh, 2020; Tauqeer et al., 2016). In order to effectively remove pollutants from water, certain plant species are utilized, i.e., Eichhornia crassipes, Ipomoea aquatica, Phragmites australis, Potamogeton natans, Ruppia maritima, Vallisneria americana, Hygrophila corymbosa, Nuphar lutea, Salvinia minima, Pistia stratiotes, and Lemna minor (Wei et al., 2021). The impact of certain bacterial species, which are associated with the growth of plants underground, can enhance plant development, promote metal translocation within the plant, alter the bioavailability of metals in the soil, and reduce metal phytotoxicity. This leads to an increase in the effectiveness of phytoremediation. Evidence from a few research shows that bacterial inoculations considerably alter the expression pattern of various metal transporters, including the ZIP, NRAMP, HMA, F-box, and AtALS3 gene families, employing these shared and unique growth-promoting functions (Dash and Osborne, 2023; Dash et al., 2018; Manobala et al., 2021; Dash and Osborne, 2023).

In Arabidopsis tissues, Bacillus amyloliquefaciens alters the transcriptional activity of the IRT1, FRO2, and FIT1 genes, increasing Fe and Cd accumulation (Sukweenadhi et al., 2015). It has been shown that the endophytic Pseudomonas fluorescens Sasm05 strain significantly increases Cd accumulation and tissue growth after inoculation, a process that mimics the overexpression of the SaHMAs, SaNRAMPs, and SaZIPs gene families (Chen et al., 2017). Much research has been conducted on the ZIP transporter gene family, which regulates zinc transportation through membranes and cytoplasmic concentrations in plant cells. Enterobacter cloacae–Zn solubilizing bacterial inoculation in rice plants had altered OsZIP1, OsZIP4, and OsZIP5 gene expression, resulting in enhanced Zn accumulation in plant tissues (Krithika and Balachandar, 2016). In Arabidopsis thaliana (Sukweenadhi et al., 2015), inoculations with Plant Growth-Promoting Rhizobacteria (PGRP) under Aluminum (Al) stress offer a promising strategy to alleviate heavy metal toxicity and enhance plant development. This is achieved by modulating the expression of key genes, including AtAIP, AtALMt1, and AtALS3. Notably, the activation of AtALS3 gene in response to Al stress results in synthesizing an ABC transporter-like protein within phloem cell membranes. This protein aids in effectively relocating Aluminum away from vulnerable areas, thus protecting the plant. While the specific role of the AtALP gene in Aluminum tolerance remains uncertain, it likely contributes to the overall adaptive response. Additionally, the collaboration between the HMA gene family and AtALS3 plays a vital role in facilitating the translocation of Heavy Metals (HMs) from the plant’s roots to the shoots, primarily accomplished through the xylem. This mechanism assists in regulating the distribution of HMs within the plant, ultimately supporting its resilience to metal-induced stress.

Unfortunately, plant cells do not include any natural transporters specific to organic environmental pollutants. Hence, they move around without actively doing anything. Root microbiome components such as rhizosphere bacteria and endophytes have long been appreciated for their role in the phytoremediation of PAHs. Diesel-contaminated soil remediation using petroleum hydrocarbons was less harmful due to the presence of endophytic microbial species such as Stenotrophomonas spp., Pseudomonas spp., Pantoea spp., and Flavobacterium spp (; Pinel-Cabello et al., 2023). To remove organic pollutants from the environment, rhizobial symbiotic consortiums use organic molecules as a C and N source in phytoremediation. Rhizobium strains that nodulate the hyperaccumulator plant Leucaena have been shown to aid in rhizoremediation by using plant toxins (such as the aromatic chemical Mimosine) as C and N sources (Sytar et al., 2021). The bacterial species help plants detoxify HMs and PAHs by increasing their metabolic growth rate. Plant growth and metabolic gene regulation by PGPR inoculations facilitate the systematic development of plant physiology (specifically, “biomass, bushiness, lateral root production, lateral root number, surface area, and thickness”). Inoculating rice seedlings with Bacillus altitudinis, for instance, improves root architecture by regulating auxin metabolism and modulating the expression of OsIAA1, OsIAA4, OsIAA11, and OsIAA13 (). The antioxidant defenses of the host plant are also strengthened by PGPR inoculations, making them more effective in combating stress.

The improvement of Solanum tuberosum Zn tolerance by Bacillus isolates is achieved by adjusting the expression of SOD, GR, DHAR, CAT, and APX genes (Gururani et al., 2013). Moreover, the growth-promoting qualities of ACC-deaminase are critical in aiding hosts to resist the toxicity of petroleum hydrocarbons, which is just one of the many ways endophytic bacteria can help. The use of arbuscular mycorrhizal fungus (AMF) and endophytic fungi to bio-enhance plant growth is a current focus in phytoremediation (Kumar and Saxena, 2019; Ordookhani et al., 2010). The underground network of mycelium belonging to AMF aids in phytoremediation by expanding the rhizosphere, enabling plants to access contaminants and nutrients. This is facilitated by a symbiotic relationship between AMF species, such as Rhizophagus irregularis, Glomus versiforme, and Funneliformis mosseae, which can increase the GRSP (Glomalin related soil protein) in soil (González-Chávez et al., 2004). As a direct result of this, the levels of lead and cadmium in maize decrease while the pH of the soil rises.

To further reduce heavy metal toxicity on host plants, AMF secrete extracellular polymeric substances (EPS) from their fungal surface through surface precipitation, ion exchange, and chelation (More et al., 2014; Riaz et al., 2021). EPS can absorb minerals and elements that are smaller than plant roots. Recent research suggests that phosphate groups with negative charges can cause Cr (III) to precipitate on the surface of fungi (Wu et al., 2021). The importance of glomalin and organic acid excretion by fungi and plants cannot be overstated when it comes to immobilizing 85% of heavy metals (HMs) in soil. By manipulating endophytic fungi, it is possible to minimize metal toxicity to plants, and some of these fungi can even flourish in environments rich in metals. Endophytic fungi possess a range of tolerance mechanisms contributing to their effectiveness in phytoremediation. These mechanisms include extracellular metal sequestration and precipitation, internal metal sequestration and complexation, compartmentation, volatilization, and metal binding to fungal cell walls. Such diverse strategies bolster the potential of phytoremediation efforts (; Sharma and Kumar, 2021). The Festuca pratensis and Festuca arundinacea, infested with endophytic fungi, grew more biomass in their roots and shoots while significantly degrading the petroleum hydrocarbons in the soil despite growing in ancient petroleum-contaminated soil (Soleimani et al., 2010). The gibberellin-producing endophyte Penicillium janthinellum LK5 protects host plants from Cd-induced oxidative stress and membrane damage by decreasing lipid peroxidation and electrolytes and increasing reduced glutathione content and catalase activity (Khan et al., 2014). Canola biomass and Cd extraction efficiency were both increased when the endophytic fungus Lasiodiplodia sp. MXSF31 was introduced to Portulaca oleracea stems grown in Pb and Cd-contaminated soils (Zanganeh et al., 2022).

4.3 Nanoparticle-soil systems

Nanotechnology has become an essential tool to overcome various agricultural restrictions, including improving nutrient utilization efficiency, reducing toxicity from heavy metals, and enhancing soil fertility through bio-nano formulations (Dave and Chopda, 2014). Sustainable nano-formulations have been shown to improve both plant health and yield. However, the disproportionate usage of nanoparticles (NPs) in numerous fields has contributed to the buildup of these particles in soils, which kill microbiota and plant systems like heavy metals (Malik et al., 2022). Despite these challenges, the soil’s physicochemical and biological properties can influence the microbiome’s ecophysiology and the stability, toxicity, complexation, and mobility of NPs. NPs accumulated in soil can undergo biological, chemical, and physical changes when interacting with soil systems’ inorganic and organic components. Physical phenomena such as aggregation can reduce the mobility of NPs in soils, whether through hetero or homo interactions between the ambient particles and NPs (; Goswami et al., 2022; Malik et al., 2022; Chebotaryova et al., 2023).

Furthermore, chemical changes to NPs can occur through surface dissolution, coating degradation, surface modification, abiotic and biotic routes, oxidation, and reduction. These changes are crucial in understanding the behavior of NPs in the soil and their potential impact on plant and soil health. Overall, the use of nanotechnology in agriculture has promising benefits, but careful consideration and monitoring of the behavior of NPs in the soil are necessary to minimize any potential adverse effects (Usman et al., 2020). Soil organic matter (SOM) has a role in the stabilization and absorption of NPs, making it one of many elements that affect their nature (stability and mobility), aggregations, and cohesiveness. Nanoparticles (NPs) can have their potential impacts mitigated by being absorbed by SOM, reducing the NPs’ surface-active area. Soil organic matter (SOM) has been found to increase the solubility of NPs in soil; for instance, CuO NPs were more soluble after SOM addition (Fato et al., 2019; Hemlata et al., 2020).

4.3.1 In what ways do nanoparticles and metals interact?

Heavy metals (HMs) and nanoparticles (NPs) coexist in agricultural settings can have devastating consequences for the soil, crop yields, and microbiota. However, the behavior of NPs can be influenced by several biological and environmental factors due to their distinct physicochemical properties. Therefore, various biotic variables may affect the interaction between HMs and NPs (da Silva et al., 2023; Sabourian et al., 2020). Moreover, the uptake, transport, and accumulation of NPs in different plant organs are also influenced by biotic factors. When present in polluted areas, heavy metals interact with NPs through physical adsorption, chemical interactions, and electrostatic binding (Noman et al., 2020). Such interactions can significantly impact the environment, accumulating these harmful substances in the soil and the food chain. Therefore, it is essential to understand the complex interactions between HMs and NPs in agricultural settings to minimize their adverse effects on the environment and public health. Examples include the adsorption of Cd from the soil by FeO NPs, which were able to do so because of their unique qualities, including reactivity, electrostatic attraction, a wide surface area, and the ability to cap molecules (Manzoor et al., 2021). In this situation, Ca and Fe transporters bring Cd into plant cells. This results in a lower metal concentration within the plant tissues as Cd and FeO NPs compete to enter the plant systems via the same transporter channel ().

Similarly, Noman et al. (2020) found that Cu-NPs reduced Cd translocation from soil to aerial parts of wheat because of their wide surface area, reactivity, and electrostatic attraction. Hence, the biogenic CuNPs’ capping molecules boosted soil Cd immobilization. As a result, the wheat’s development was aided by the plant’s ability to absorb Cu-bound nutrients. It functions as a coenzyme in essential reactions and stimulates plant growth and development in polluted soil. As another example, graphene oxide (GO), which has a similarly huge surface area, has been utilized to clean up HMs contaminated areas (Etemadi et al., 2017). For instance, graphene oxide sheets, which, due to their functional group, may conjugate with metals like Cr (VI), speed up the adsorption kinetics of HMs ions (Wang et al., 2017). In conclusion, NPs’ metal complexing abilities are anticipated to aid in elucidating how the NPs may effectively reduce metal toxicity.

4.3.2 Techniques for reducing exposure to hazardous metals using nano-bioremediation

Across the globe, researchers have employed multiple approaches, such as physical, chemical, and biological techniques - including phyto and microbial remediation - to decontaminate soil polluted with heavy metals (Yadav et al., 2017; Singh et al., 2020; Sunanda et al., 2022). This is done to ensure that the soil becomes suitable for farming, considering the risks heavy metals pose to diverse life forms. Nevertheless, most of these techniques have only been tested in the lab at bench scales, and those tested in real-world settings have met with scant success for various reasons. Physicochemical methods include excavation and landfill (Funtikova et al., 2023), chemical reduction, evaporation acid leaching, soil washing, soil flushing, precipitation, electrokinetic extraction, vitrification, thermal treatment, and surface capping pose significant issues as mentioned in Table 9 (Rahman and Singh, 2020). The adverse impacts on soil, microbiota, and plant ecosystems are a direct result of the production of secondary metabolites, which can be costly and difficult to eradicate (Gaur et al., 2014; Wang P. et al., 2018). Table 10 outlines the utilization of nanoparticles in the remediation of heavy metals (HMs) and persistent organic pollutants (POPs), showcasing their efficacy in tackling environmental contaminants through innovative nanotechnology-based solutions.

TABLE 9

Bioremediation processOptimal conditions (°C)Key microorganisms involvedCommon pollutants treatedKey considerations
BiostimulationNutrient addition (N, P), moisture: 15%–30%, pH: 6–8, temperature: 15–45Indigenous soil bacteria and fungiHydrocarbons, petroleum products, pesticidesEnsure adequate nutrient and moisture levels
BioaugmentationSpecific pollutant presence, pH: 6–8, temperature: 20–35Introduced specialized bacteria or fungi (e.g., Pseudomonas, Phanerochaete chrysosporium)PCBs, chlorinated solvents, hydrocarbonsSelect appropriate microbial strains for specific pollutants
PhytoremediationSunlight, nutrient-rich soil, pH: 5–7, temperature: 15–30Plants (e.g., poplar trees, sunflowers, Indian mustard)Heavy metals, radionuclides, organic contaminantsChoose plants with deep roots and high biomass
BioventingAerobic conditions, pH: 6–8, moisture: 10%–20%, temperature: 15–35Indigenous soil bacteria and fungiVolatile organic compounds (VOCs), hydrocarbonsEnsure sufficient oxygen supply and monitor gas emissions
BiospargingAerobic conditions, Groundwater table control, pH: 6–8, temperature: 10–25Indigenous or introduced aerobic bacteriaVOCs, BTEX (benzene, toluene, ethylbenzene, xylene)Optimize air injection rate and pressure
CompostingAerobic conditions, Moisture: 40%–60%, pH: 5.5–8.5, temperature: 40–60Thermophilic bacteria and fungiOrganic wastes, explosives, petroleum hydrocarbonsMaintain proper aeration, temperature, and moisture levels
LandfarmingAerobic conditions, Moisture: 15%–30%, pH: 6–8, Temperature: 15–35Indigenous soil microorganismsPetroleum hydrocarbons, pesticides, heavy metalsRegularly till soil to maintain aeration and monitor contaminant levels

Summary of the optimal conditions required for different types of bioremediation processes (; ; Cepoi et al., 2022; Goswami et al., 2022; Chebotaryova et al., 2023).

TABLE 10

Nanoparticle typeMechanism for HMs remediationMechanism for POPs remediationTarget contaminants (examples)
Metal Oxides (e.g., iron oxide, aluminum oxide)* Adsorption: high surface area allows for physical binding of HMs. * Surface complexation: functional groups on the nanoparticle surface complex with HMs, reducing mobility. * Precipitation: nanoparticles can induce precipitation of less soluble HM forms.* Adsorption: organic pollutants can adhere to the nanoparticle surface through hydrophobic interactions. * Degradation: some metal oxides have catalytic properties that degrade organic pollutants.As, Pb, Cd, Cr, PCBs, PAHs
Metal sulfides [e.g., zero-valent iron nanoparticles (nZVI)]* Reduction: nZVI can reduce Cr(VI) to the less mobile Cr(III). * Sulfidation: react with dissolved metal ions to form insoluble metal sulfides.* Dechlorination: can break down chlorinated organic pollutants by removing chlorine atoms.Cr, Hg, Pb, Cd, PCBs, DDT
Carbon nanomaterials (e.g., carbon nanotubes, fullerenes)* Adsorption: large surface area for strong adsorption of both HMs and organic pollutants. * Encapsulation: can encapsulate pollutants within their structure, preventing further interaction with the environment.* Degradation: some carbon nanomaterials exhibit catalytic activity for POP degradation.As, Pb, Hg, PAHs, PCBs
Biopolymeric Nanoparticles (e.g., chitosan nanoparticles)* Chelation: functional groups on the nanoparticle bind HMs through chelation, reducing mobility. * Biodegradation: enhance microbial degradation of pollutants by providing a surface for attachment and colonization.* Adsorption: can adsorb organic pollutants through various interactions.As, Cd, Pb, PAHs, Pesticides
Dendrimers (synthetic polymers with a branched structure)* Size-exclusion: can trap HMs within their internal cavities due to size limitations. * Surface modification: functional groups on dendrimers can be tailored for specific HM binding.* Encapsulation: encapsulate organic pollutants within their cavities, preventing environmental release. * Solubilization: enhance solubility of hydrophobic POPs.Pb, Cd, Hg, PAHs, PCBs

Nanoparticles for remediation of heavy metals (HMs) and persistent organic pollutants (POPs) (Gaur et al., 2014; Wang et al., 2018; Singh et al., 2020; Sunanda et al., 2022; Yadav et al., 2017; Fulekar et al., 2012; Gavrilescu, 2022; Oladoye et al., 2022).

For instance, According to Lambert et al. (2000), FRTR (Federal Remediation-Technologies Roundtable) statistics suggest that excavation and disposal costs $270 to $460 per tonne (Feng et al., 2020; Hu et al., 2021). The United States Environmental Protection Agency (USEPA) estimates that, depending on the size of the polluted site, the cost of soil cleaning ranges from $150 per tonne up to $250 per tonne.

Selection and placement of plants, irrigation, soil amendment, field monitoring, harvesting, and residue management all add to the price tag of a treatment that relies on phytoextraction. The cost of remediation could range from $10 to $35 per ton of soil with low levels of toxins, which also depends on the contamination level and size of the site (

Fulekar et al., 2012

). Due to the plant-based nature of phytoremediation, the soil treatment process, which typically takes 3 months to 5 years, becomes more expensive and time-consuming (

Gavrilescu, 2022

;

Oladoye et al., 2022

). However, the clean-up has failed under natural field conditions due to reliance on specific pollutant characteristics, soil qualities, low efficiency, changing environments, and site conditions. Metal clean-up programs rely heavily on nanotechnology because of the unique physicochemical properties of nanosized particles (NPs) ranging in size from 1 to 100 nm. Furthermore, the nano remediation procedure has successfully removed heavy metals from soil ecosystems and other habitats by exploiting NPs’ potential mobility, reactivity (catalysis), and adsorption properties (

Corsi et al., 2018

;

;

Del Prado-Audelo et al., 2021

). Nanoremediation technology is one of the most promising remediation alternatives, and it removes toxic metals through a variety of mechanisms, including

  • (i) absorption,

  • (ii) oxide reduction to a stable metallic state,

  • (iii) heterogeneous catalysis,

  • (iv) deployment of electrical fields (electro-nano remediation),

  • (v) photodegradation, and

  • (vi) the use of biological materials (nano-bioremediation).

Various materials such as polymers, carbon-based compounds, metallic oxides, metals, and nanocomposites have remarkably removed metals (). However, the type of metal and pollution source (e.g., biogenic) can affect the efficacy of these materials. Such materials include carbon nanoparticles (fullerenes), semiconductors, noble metals, and magnetic nanoparticles (such as zinc oxide and titanium dioxide). One specific example is Spirulina platensis supported PdNP, which removed between 12%–90% of Pd from polluted environments (Sayadi et al., 2018). On the other hand, an iron oxide nanoparticle-based on Geobacter sulfurreducens could remove chromium from chromium-polluted soils altogether (O’Neil et al., 2008). Overall, these findings highlight the potential of using different materials and approaches for effective metal removal, which could be tailored based on the type of pollutant and the specific environmental conditions. Nanoscale metal oxide particles (MONPs) made of iron, silver, nickel, and palladium have been remarkably successful in removing toxic metals and other chemicals from polluted areas. Detoxifying Cd stress in wheat plants using FeO NPs increased plant growth, antioxidants, and chlorophyll levels (Manzoor et al., 2021). Cd-phosphate production appears to be the leading cause for decreased bioaccumulation of Cd in soil, and treatment of the soil with Fe3 (PO4)2 NPs successfully immobilized the Cd by 70% (Gong et al., 2018).

Similarly, another study found that applying biochar-supported FeNPs reduced plant Cr bioavailability (Neeli et al., 2020). Wheat’s development and nutrient profile were found to be improved when Cu NPs were present, and vice versa (Noman et al., 2020). Notwithstanding the progress, new NPs that are effective in nano remediation technologies must be discovered. However, this requires researchers to collaborate with local governments, which can back innovations and fund research to identify sustainable nano-solutions for contaminated soils. Compared to traditional clean-up methods, nano remediation technology is typically swift, may be deployed over a broad contamination region, and costs less. According to the USEPA, about 70 potentially harmful trace elements have been effectively cleaned worldwide using nano-remediation techniques, considerably reducing time and operational costs (Feng et al., 2023; Tufail et al., 2022; Yang et al., 2023).

4.3.3 Microbiome-mediated nano-bioremediation of toxic metals

Microbes have long been used in various settings, including the medical, agricultural, and environmental sectors. However, as explained below, the application of microbiome to further optimize nanoparticle usage in the nano-bioremediation process has also shown promising results in detoxifying various inorganic contaminants, hence reducing the limiting potential of bioremediation (). Microbiome-based nano-bioremediation has demonstrated substantial progress in detoxifying carcinogenic and mutagenic chromium by employing palladium nanoparticles (). These nanoparticles are synthesized using Pd (II) ions, with the mediation of Clostridium pasteurianum. The process involves the conversion of hexavalent chromium into an insoluble trivalent form, resulting in hydrogen gas production.

Similarly, a matrix composed of carbon nanotubes (CNTs), sodium alginate, and polyvinyl alcohol (PVA) immobilized on P. aeruginosa has been shown to detoxify Cr (VI) selectively (Pang et al., 2011). At 80 mg/L Cr (VI), the immobilized bacterial cells converted 84% of the compound to the soluble Cr (III), and this process was completed within 24 h. Biotransformation of poisonous Cr (VI) into less harmful Cr (III) has been demonstrated by immobilised cells of Shewanella oneidensis stabilised with CNTs (Yan et al., 2013). Immobilized S. oneidensis and carbon nanotubes were four times more effective at removing hexavalent chromium from a solution than the test bacteria or calcium alginate beads alone. Based on these results, it is plausible that nano-bioremediation methods targeting habitats contaminated with inorganic pollutants could benefit from incorporating CNTs with bacteria. Magnetic iron oxide nanoparticles, known as MIONPs, have become popular for removing metals due to their extensive surface area, strong reactivity, adjustable features, distinctive magnetic qualities, potent reducing ability and capacity to soak up various dangerous metals and metalloids (Kumar et al., 2019; Verma et al., 2023). For instance, the Lysinibacillus sphaericus prepared magnetic oxide nanoparticles have been shown to release exopolysaccharides (EPS) that act as a complexing, stabilizing, and capping agent and have several binding sites for different metal ions. The EPS-functionalized magnetic oxide nanoparticles (VI) improve the ability to absorb Cr (Kumar et al., 2019).

Similarly, adding iron nanoparticles, produced by Chlorococcum sp. green algae, led to a 92% reduction of Cr (VI) to Cr (III). These nanoparticles were highly reactive, stable, and had a practical ability to reduce (Subramaniyam et al., 2015). Further strengthening algae’s role in detoxifying carcinogenic chromium is the incorporation of C. vulgaris as a functionalized agent in ultrafine bi-metallic (TiO2/Ag) chitosan nanofiber mats. According to this study, combining C. vulgaris algae with TiO2/Ag chitosan nanofiber mats significantly boosted the photocatalytic reduction of hexavalent chromium. The researchers observed that various organic compounds secreted by the algae played a crucial role in enhancing the process. As a result, the study implies that the synergistic effect between the algae and TiO2/Ag hybrid nanomaterial could offer a cost-effective solution for removing chromium from polluted environments (Goher et al., 2016; ). Rhodosporidium diobovatum was responsible for generating lead sulfide (PbS) nanoparticles, which effectively converted toxic Pb (II) ions into less harmful and advantageous compounds (Seshadri et al., 2011). Combining B. subtilis and nanohydroxyapatite and the production of CdS nanoparticles from P. aeruginosa (NHAP) successfully eliminated Cd from a Cd-contaminated environment. Implementing this remediation approach stimulated the rhizosphere community, leading to a notable rise in bacterial diversity in rapeseed (Brassica campestris L.) cultivated in previously contaminated soil (Liu et al., 2018).

4.3.4 Nanoparticles in remediation of POPs

Economic and technological variables must be considered when selecting a treatment technique for POP removal, as they significantly impact POP destiny, transport, and degradation (Zhou et al., 2023). With the rise of nanotechnology, a powerful tool is now available to tackle environmental problems, specifically in purifying polluted treatment solutions. Nanoremediation is a state-of-the-art method that may safely and effectively remove organic contaminants from the environment. Nanomaterials are highly beneficial in many fields due to their extraordinary electromagnetic, structural, mechanical, thermal, and optical capabilities, i.e., in wastewater treatment (Del Prado-Audelo et al., 2021). Various forms of nanomaterials can be created through different methods, including physical, chemical, or biological processes. Many researchers also utilize green chemistry principles to ensure environmentally friendly synthesis. Cutting-edge multifunctional nanomaterials such as nanowires, nanoflowers, and nanocomposites are designed to optimize performance and address existing obstacles (Corsi et al., 2018). Higher specific surface area (SVR) of nanomaterials enhances their reactivity with POPs. In the upcoming sections, we will delve into nanocatalysis, nano adsorbents, and nanomembranes in POP treatment.

4.3.4.1 Nanocatalysis

Traditional technologies have proven ineffective in completely breaking down and eliminating organic pollutants, leading to a need for a more sustainable approach that minimizes energy and chemical consumption. Exploring advanced oxidation processes (AOPs) as cost-effective solutions due to their powerful oxidizing radicals. Nanocatalysis has emerged as a promising approach for transforming contaminants into eco-friendly compounds by utilizing semiconducting wide-bandgap nanomaterials (). Metal and metal-oxide nanomaterials are increasingly recognized for their potential in addressing persistent organic pollutants (POPs) sustainably. Different nanocatalysts, such as Fenton-based, electrocatalytic, and photocatalytic, are used to degrade POPs. Photocatalysis, a widely recognized advanced oxidation process (AOP), utilizes light to activate nanocatalysts, producing reactive oxygen species (ROS) that efficiently break down organic pollutants (Fei et al., 2022). This process is highly effective in dealing with volatile organic compounds (VOCs) such as Dioxins and polychlorinated biphenyls (PCBs) by producing free radicals. When certain nanocatalysts, like ZnO, TiO2, or WO3, are exposed to light and oxygen, they become excited and can break down POPs through photocatalysis. Currently, TiO2 and ZnO are the primary semiconductors employed to degrade POPs (Nandini et al., 2023). Their ability to effectively remove highly hydrophobic POPs is impressive. Important considerations for catalyst selection involve surface characteristics, pore volume, and material structure. Optimizing surface properties and crystal structure improves degradation efficiency. On the other hand, one downside of photocatalysis is the difficulty in eliminating nanomaterial after the reaction.

Lwin et al. (2019) previously produced a cube-shaped ZnO-SnO2 nanocomposite, showing that it effectively degraded tetracycline hydrochloride. This material showed exceptional photostability throughout its four cycles, which suggests it is suitable for its potential use in cleaning up organic pollutants like POPs. introduced a nanocatalyst designated MnFe2O4@PANI@Ag to break down azo dye in their investigation. This nanocatalyst has demonstrated sustained performance during numerous cycles and has the added benefit of being quickly separated with an external magnet. Khan et al. (2018) developed a magnetic Fe-ZnO nanocomposite that efficiently removed the insecticide Chlorpyrifos. Keeping its excellent stability and reusability, the nanocomposite showed remarkable performance, degrading the pesticide quickly. A recent study by Chen et al. (2022) focused on Mn-based nanocomposites and their ability to degrade bisphenol A. The researchers found that these nanocomposites exhibited impressive mineralization and BPA removal efficiency, maintaining their high performance even after multiple cycles. Photocatalysis is a popular choice for wastewater treatment due to its high efficiency and sustainability in combating a wide range of pollutants.

4.3.4.2 Nanoadsorption

With their extensive surface area, adjustable pore size, minimized intraparticle-diffusion distance, and powerful surface activity, nano adsorbents demonstrate exceptional sorption efficiency, effectively trapping a diverse range of pollutants. They can be easily tailored to target specific pollutants, which enhances their selectivity. This technology has effectively eliminated persistent organic pollutants (POPs) such as hydrocarbons, dyes, phenols, and pesticides (Chen et al., 2022). Nanoadsorption has proven to be a highly effective technique for POP remediation by utilizing electrostatic, hydrogen bonding, and hydrophobic interactions. Numerous nanomaterials, such as carbon-based nanomaterials, metal oxides, zeolite, and clay, are widely used in this process. Introducing innovative magnetic separation strategies, magnetic nanoparticles, especially iron oxide, play a crucial role. The microporous structure of activated carbon improves the efficiency of removing POPs, while nano adsorbents made from carbon can interact with contaminants. Carbon nanotubes can significantly boost their adsorption capacity with surface modifications, making them highly efficient in removing pollutants. The adsorption of cyanazine through iron nanocomposites produced using green technologies was examined in a study by . The results showed that cyanazine was rapidly removed, which can be attributed to the short contact time. In recent years, Mahdavi et al. (2021) successfully applied magnetic-graphene oxide treated with amino-guanidine to eliminate chlorpyrifos pesticide. The researchers observed significant desorption through HPLC-MS analysis using a synthesized nano adsorbent. In a recent study, Izanloo et al. (2019) created a nano adsorbent (Fe3O4@SiO2@NH2@SH) that effectively removed 2,4-D and lead from contaminated environments. The researchers found that the pH level played a critical role in the adsorption of organic contaminants.

Additionally, the nano adsorbent demonstrated consistent desorption efficiency even after multiple cycles. In a recent study, Mohammadi et al. (2018) researched a modified magnetic nano adsorbent. They focused on its ability to rapidly separate pollutants and effectively remove phenoxy-acid herbicides such as 2,4-D and MCPA. Dehghani et al. (2019) evaluated the potential of multi-walled carbon nanotubes (MWCNTs) to remove the herbicide diazinon. They discovered that at pH 6, diazinon was completely removed after 15 min, demonstrating the efficacy of MWCNTs in pesticide cleanup. Utilizing nano adsorbents in wastewater treatment can provide a practical and environmentally friendly approach to removing heavy metals. Additionally, the magnetic variants of these adsorbents can be conveniently separated using external magnets, resulting in reduced operational expenses.

4.3.4.3 Nanofiltration

The introduction of nanofiltration membranes has significantly transformed water treatment systems, bringing about a revolution in nanotechnology. These membranes, along with microfiltration (MF), reverse osmosis (RO), and ultrafiltration (UF), provide highly efficient methods for wastewater treatment, offering alternatives to conventional techniques. Membrane processes are known for their remarkable removal efficiency, especially in organic micropollutants, although they can be quite expensive (Corina-Petronela and Teodosiu, 2007). Their functionality is significantly enhanced by incorporating nanoparticles into membranes using different techniques such as surface immobilization or blending. Electrospinning allows the creation of polymeric or composite nanofibrous membranes that provide incredibly precise filtration ranging from 10 to 1,000 nm. Micro/trace organic pollution can be effectively filtered using membrane techniques like reverse osmosis (RO) and nanofiltration (NF). NF, in particular, is known for its effectiveness thanks to its smaller pore sizes and user-friendly nature (Tibi et al., 2020). Nanofiltration membranes are constructed using a variety of polymers, some of which are naturally occurring and others of which are synthetic. These comprise polyvinyl fluoride, polypropylene, polyacrylonitrile, and cellulose acetate. With their stable adsorption structures, nanofibers effectively eliminate pesticides from wastewater through molecular propagation. Incorporating semiconducting materials into nanofibers enhances their efficiency in dye compound remediation by giving them photocatalytic properties (Oatley-Radcliffe et al., 2017). These nanocomposite nanofiber membranes, such as ZnO-cellulose acetate and TiO2-graphene, exhibit remarkable photocatalytic efficiency. In addition, combining magnetic nanoparticles with membranes and adding TiO2 can significantly improve the ability to remediate organic pollutants.

Different filtration techniques, such as ultrafiltration, microfiltration, and nanofiltration, are used to eliminate organic and inorganic pollutants effectively. When combined with biological or chemical methods, filtration can significantly improve the efficiency of remediation. However, the success of this approach depends on various factors, including the type of membrane, modules, composition, and how well it interacts with pollutants. Using pressure dynamics, nanofiltration efficiently targets compounds with low molecular weight (1–10 nm) and reduces the hardness of organic pollutants, decreasing ionic strength. Electrospinning creates nanofibrous membranes that are essential for achieving optimal filtration performance. Nanofiltration is an excellent method for removing arsenic from water because it can effectively separate soluble minerals and other ions.

Karimi-Shamsabadi et al. (2016) examined the efficacy of a thin-film composite poly-amide nanofiltration membrane in removing atrazine and diazinon from wastewater. The researchers found that the membrane had a higher rejection rate for diazinon than atrazine. The modified membranes showed improved water permeability and diazinon rejection, suggesting better pesticide removal performance. In a recent study, Wang et al. (2020) introduced a new type of nanocomposite catalyst. This catalyst, called Al-MOF/Fe3O4/PDA@Ag, contains silver nanoparticles and has shown impressive performance in eliminating organic pollutants such as CIP, NOR, and MO. One of the notable advantages of this catalyst is its ability to be easily separated using an external magnet. Additionally, it has demonstrated good reusability and stability, making it a promising option for future applications. Membrane filtration, especially nanofiltration, is widely acknowledged as a secure technology for effectively eliminating low-molecular-weight compounds and pesticides. However, the issue of membrane fouling remains a persistent challenge that can be overcome by utilizing blended techniques.

5 Factors affecting bioremediation

Bioremediation, the process of using living organisms to remove or neutralize contaminants from the environment, is influenced by many factors. These factors can significantly impact the efficiency and effectiveness of bioremediation efforts (Yang Y.-C. et al., 2020). Understanding these factors is crucial for designing and implementing successful bioremediation strategies. One of the primary factors affecting bioremediation is the type and concentration of contaminants present in the environment. Different contaminants require specific microbial communities and enzymatic pathways for degradation. For instance, hydrocarbon-degrading bacteria effectively remove petroleum-based pollutants, while heavy metal-contaminated sites may require metal-resistant bacteria or plants with metal-accumulating capabilities (Yetunde Mutiat et al., 2018).

Additionally, high concentrations of contaminants can inhibit microbial activity, so it is essential to optimize conditions to ensure microbial growth and activity. Environmental conditions such as temperature, pH, oxygen availability, and moisture content also play a critical role in bioremediation (Yadav et al., 2017). Most microbial activity occurs within specific temperature and pH ranges, and extreme conditions can hinder microbial growth and metabolism. Adequate oxygen levels are necessary for aerobic degradation processes, while anaerobic conditions may be required to reduce specific contaminants. Similarly, moisture content affects microbial activity and nutrient availability, with excessive dryness or water saturation inhibiting bioremediation processes (Wang et al., 2023).

The availability of nutrients such as carbon, nitrogen, and phosphorus is another critical factor influencing bioremediation (Tufail et al., 2022). Microorganisms require these nutrients for growth and metabolism, and their availability can limit microbial activity in contaminated environments. Supplementing nutrients through techniques like fertilization or bioaugmentation can enhance microbial growth and biodegradation rates, particularly in nutrient-poor environments. The microbial community present in the contaminated site also significantly influences bioremediation outcomes (Talukdar et al., 2020). Indigenous microorganisms may already possess the metabolic capabilities required for contaminant degradation, potentially reducing the need for external intervention. However, in some cases, the indigenous microbial community may be insufficient to effectively remediate contaminants, necessitating the introduction of specialized microbial consortia or genetically engineered microorganisms. The accessibility and permeability of the contaminated matrix also impact bioremediation efficiency. Contaminants within soil aggregates, pores, or dense matrices may be less accessible to microbial degradation, requiring physical or chemical pretreatment to enhance accessibility. Similarly, contaminants in groundwater or deep soil layers may be more challenging to reach and treat effectively (Sreedevi et al., 2022).

Furthermore, external factors such as regulatory requirements, public perception, and economic considerations can influence bioremediation project planning and implementation. Compliance with environmental regulations, stakeholder engagement, and cost-effectiveness are essential considerations in designing bioremediation strategies.

6 Conclusion

In conclusion, the issue of heavy metal and POPs pollution poses a significant threat to both the environment and human health. To address this problem, bioremediation utilizing microorganisms and plants has emerged as a promising technology to detoxify contaminated soil. Certain microorganisms and plants exhibit strong metal adsorption capabilities, making them well-suited for bioremediation efforts. However, the effectiveness of phytoremediation has been hindered by the slow growth of plants and low remediation efficiency. To overcome these limitations, using plant-associated microbes, particularly PGPR, can enhance the removal efficiency of heavy metals in contaminated soil.

Moreover, nanotechnology offers the potential to remediate hazardous metals, and integrating nanoparticles with bioremediation, known as nano-bioremediation, holds promise for removing harmful contaminants. Understanding the interactions between the soil microbiome, nanoparticles, and contaminants is pivotal for successfully implementing nano-remediation strategies and optimizing crops in contaminated fields. Overall, developing and implementing efficient and sustainable bioremediation strategies for heavy metal pollution are crucial in safeguarding the environment and human health.

Statements

Author contributions

AK: Conceptualization, Formal Analysis, Resources, Supervision, Writing–original draft. SM: Conceptualization, Formal Analysis, Resources, Writing–original draft, Validation. AD: Validation, Visualization, Writing–review and editing, Data curation. AA-T: Data curation, Writing–review and editing, Formal Analysis, Investigation, Visualization. TM: Resources, Validation, Writing–review and editing, Data curation, Formal Analysis.

Funding

The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.

Acknowledgments

I am obliged to conduct my research at Lovely Professional University, Phagwara, and Jimma University, Ethiopia.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

  • 1

    AbbasiS.ZahediH.SadeghipourO.AkbariR. (2013). Effect of plant growth promoting rhizobacteria (PGPR) on physiological parameters and nitrogen content of soybean grown under different irrigation regimes. Res. Crops14 (3), 798803.

  • 2

    AbduN.AbdullahiA. A.AbdulkadirA. (2017). Heavy metals and soil microbes. Environ. Chem. Lett.15 (1), 6584. 10.1007/s10311-016-0587-x

  • 3

    AbedinzadehM.EtesamiH.AlikhaniH. A. (2019). Characterization of rhizosphere and endophytic bacteria from roots of maize (Zea mays L.) plant irrigated with wastewater with biotechnological potential in agriculture. Biotechnol. Rep.21, e00305. 10.1016/j.btre.2019.e00305

  • 4

    AdebusuyiA. T.SojinuS. O.AleshinloyeA. O. (2022). The prevalence of persistent organic pollutants (POPs) in West Africa – a review. Environ. Challenges7, 100486. 10.1016/j.envc.2022.100486

  • 5

    AdeyemiN. O.AtayeseM. O.SakariyawoO. S.AzeezJ. O.Abayomi SobowaleS. P.OlubodeA.et al (2021). Alleviation of heavy metal stress by arbuscular mycorrhizal symbiosis in Glycine max (L.) grown in copper, lead and zinc contaminated soils. Rhizosphere18, 100325. 10.1016/j.rhisph.2021.100325

  • 6

    AgarwalM.RathoreR. S.JagoeC.ChauhanA. (2019). Multiple lines of evidences reveal mechanisms underpinning mercury resistance and volatilization by stenotrophomonas sp. MA5 isolated from the savannah river site (SRS), USA. Cells8 (4), 309. 10.3390/cells8040309

  • 7

    AhkamiA. H.Allen WhiteR.HandakumburaP. P.JanssonC. (2017). Rhizosphere engineering: enhancing sustainable plant ecosystem productivity. Rhizosphere3, 233243. 10.1016/j.rhisph.2017.04.012

  • 8

    AhmedT.NomanM.ManzoorN.ShahidM.AbdullahM.AliL.et al (2021). Nanoparticle-based amelioration of drought stress and cadmium toxicity in rice via triggering the stress responsive genetic mechanisms and nutrient acquisition. Ecotoxicol. Environ. Saf.209, 111829. 10.1016/j.ecoenv.2020.111829

  • 9

    Al-EnaziN. M.AlTamiM. S.AlhomaidiE. (2022). Unraveling the potential of pesticide-tolerant Pseudomonas sp. augmenting biological and physiological attributes of Vigna radiata (L.) under pesticide stress. RSC Adv.12, 1776517783. 10.1039/D2RA01570F

  • 10

    AlexakisD. (2016). Human health risk assessment associated with Co, Cr, Mn, Ni and V contents in agricultural soils from a Mediterranean site. Archives Agron. Soil Sci.62 (3), 359373. 10.1080/03650340.2015.1062088

  • 11

    Al-HuqailA. A.El-BondklyA. M. A. (2022). Improvement of Zea mays L. growth parameters under chromium and arsenic stress by the heavy metal-resistant Streptomyces sp. NRC21696. Int. J. Environ. Sci. Technol.19 (6), 53015322. 10.1007/s13762-021-03532-7

  • 12

    AliM.SongX.DingD.WangQ.ZhangZ.TangZ. (2022). Bioremediation of PAHs and heavy metals co-contaminated soils: challenges and enhancement strategies. Environ. Pollut.295, 118686. 10.1016/j.envpol.2021.118686

  • 13

    AlyA. H.DebbabA.ProkschP. (2011). Fungal endophytes: unique plant inhabitants with great promises. Appl. Microbiol. Biotechnol.90 (6), 18291845. 10.1007/s00253-011-3270-y

  • 14

    AmbreethaS.ChinnaduraiC.MarimuthuP.BalachandarD. (2018). Plant-associated Bacillus modulates the expression of auxin-responsive genes of rice and modifies the root architecture. Rhizosphere5, 5766. 10.1016/j.rhisph.2017.12.001

  • 15

    AmirM.KurtanU.BaykalA.SözeriH. (2016). MnFe2O4@PANI@Ag heterogeneous nanocatalyst for degradation of industrial aqueous organic pollutants. J. Mater. Sci. Technol.32, 134141. 10.1016/j.jmst.2015.12.011

  • 16

    ArifM. S.YasmeenT.ShahzadS. M.RiazM.RizwanM.IqbalS.et al (2019). Lead toxicity induced phytotoxic effects on mung bean can be relegated by lead tolerant Bacillus subtilis (PbRB3). Chemosphere234, 7080. 10.1016/j.chemosphere.2019.06.024

  • 17

    ArwidssonZ.JohanssonE.Von KronhelmT.AllardB.Van HeesP. (2010). Remediation of metal contaminated soil by organic metabolites from fungi i-production of organic acids. Water, Air, Soil Pollut.205 (1-4), 215226. 10.1007/s11270-009-0067-z

  • 18

    AsatiA.PichhodeM.NikhilK. (2016). Effect of heavy metals on plants: an overview. IJAIEM5 (3), 5666.

  • 19

    AwasthiS.ChauhanR.DwivediS.SrivastavaS.SrivastavaS.TripathiR. D. (2018). A consortium of alga (Chlorella vulgaris) and bacterium (Pseudomonas putida) for amelioration of arsenic toxicity in rice: a promising and feasible approach. Environ. Exp. Bot.150, 115126. 10.1016/j.envexpbot.2018.03.001

  • 20

    AzzamA. M.TawfikA. (2015). Removal of heavy metals using bacterial bio-flocculants of Bacillus sp. and Pseudomonas sp. J. Environ. Eng. Landsc. Manag.23 (4), 288294. 10.3846/16486897.2015.1068781

  • 21

    BallesterosS.RincónJ. M.Rincón-MoraB.JordánM. M. (2017). Vitrification of urban soil contamination by hexavalent chromium. J. Geochem. Explor.174, 132139. 10.1016/j.gexplo.2016.07.011

  • 22

    BalusamyS. R.KaruppiehS.VenkatS.ThangaveluL.KimY. J.PerumalsamyH. (2021). “Biomedical applications of ginsenosides nanoparticles synthesized using microbes,” in Agri-waste and microbes for production of sustainable nanomaterials, 625653.

  • 23

    BandaruS. R. S.Van GenuchtenC. M.KumarA.GladeS.HernandezD.NahataM.et al (2020). Rapid and efficient arsenic removal by iron electrocoagulation enabled with in situ generation of hydrogen peroxide. Environ. Sci. Technol.54 (10), 60946103. 10.1021/acs.est.0c00012

  • 24

    BanoA.HussainJ.AkbarA.MehmoodK.AnwarM.HasniM. S.et al (2018). Biosorption of heavy metals by obligate halophilic fungi. Chemosphere199, 218222. 10.1016/j.chemosphere.2018.02.043

  • 25

    BaragañoD.ForjánR.WelteL.GallegoJ. L. R. (2020). Nanoremediation of as and metals polluted soils by means of graphene oxide nanoparticles. Sci. Rep.10 (1), 1896. 10.1038/s41598-020-58852-4

  • 26

    BaranM. F.DuzM. Z. (2021). Removal of cadmium (II) in the aqueous solutions by biosorption of Bacillus licheniformis isolated from soil in the area of Tigris River. Int. J. Environ. Anal. Chem.101 (4), 533548. 10.1080/03067319.2019.1669583

  • 27

    BarkerA. V.BrysonG. M. (2002). Bioremediation of heavy metals and organic toxicants by composting. ScientificWorldJournal2, 407420. 10.1100/tsw.2002.91

  • 28

    BarnawalD.BhartiN.PandeyS. S.PandeyA.ChanotiyaC. S.KalraA. (2017). Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol. Plant.161 (4), 502514. 10.1111/ppl.12614

  • 29

    Barra CaraccioloA.TerenziV. (2021). Rhizosphere microbial communities and heavy metals. Microorganisms9 (7), 1462. 10.3390/microorganisms9071462

  • 30

    BaruahN.MondalS. C.FarooqM.GogoiN. (2019). Influence of heavy metals on seed germination and seedling growth of wheat, pea, and tomato. Water, Air, Soil Pollut.230 (12), 273. 10.1007/s11270-019-4329-0

  • 31

    BeczeA.VinczeÉ. B.VargaH. M.GyöngyvérM. (2021). Effect of plant growth promoting rhizobacteria on zea mays development and growth under heavy metal and salt stress condition. Environ. Eng. Manag. J.20 (4), 547557. 10.30638/eemj.2021.053

  • 32

    BelimovA. A.ShaposhnikovA. I.AzarovaT. S.MakarovaN. M.SafronovaV. I.LitvinskiyV. A.et al (2020). Microbial consortium of PGPR, rhizobia and arbuscular mycorrhizal fungus makes pea mutant SGECdt comparable with indian mustard in cadmium tolerance and accumulation. Plants9 (8), 9751021. 10.3390/plants9080975

  • 33

    BhatiR.SreedharanS. M.RizviA.KhanM. S.SinghR. (2022). An insight into efflux-mediated arsenic resistance and biotransformation potential of Enterobacter cloacae RSC3 from arsenic polluted area. Indian J. Microbiol.62 (3), 456467. 10.1007/s12088-022-01028-7

  • 34

    BhattP.PandeyS. C.JoshiS.ChaudharyP.PathakV. M.HuangY.et al (2022). Nanobioremediation: a sustainable approach for the removal of toxic pollutants from the environment. J. Hazard. Mater.427, 128033. 10.1016/j.jhazmat.2021.128033

  • 35

    BhattacharyaS.DasA.PrashanthiK.PalaniswamyM.AngayarkanniJ. (2014). Mycoremediation of Benzo[a]pyrene by Pleurotus ostreatus in the presence of heavy metals and mediators. 3 Biotech.4 (2), 205211. 10.1007/s13205-013-0148-y

  • 36

    BobakerA. M.AlakiliI.SarmaniS. B.Al-AnsariN.YaseenZ. M. (2019). Determination and assessment of the toxic heavy metal elements abstracted from the traditional plant cosmetics and medical remedies: case study of Libya. Int. J. Environ. Res. Public Health16 (11), 1957. 10.3390/ijerph16111957

  • 37

    BoenteC.SierraC.Rodríguez-ValdésE.Menéndez-AguadoJ. M.GallegoJ. R. (2017). Soil washing optimization by means of attributive analysis: case study for the removal of potentially toxic elements from soil contaminated with pyrite ash. J. Clean. Prod.142, 26932699. 10.1016/j.jclepro.2016.11.007

  • 38

    BriffaJ.SinagraE.BlundellR. (2020). Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon6 (9), e04691. 10.1016/j.heliyon.2020.e04691

  • 39

    BrimH.VenkateswaranA.KostandarithesH. M.FredricksonJ. K.DalyM. J. J. A.microbiologye. (2003). Engineering Deinococcus geothermalis for bioremediation of high-temperature radioactive waste environments. Appl. Environ. Microbiol.69 (8), 45754582. 10.1128/aem.69.8.4575-4582.2003

  • 40

    ÇabukA.AkarT.TunaliS.TabakO. (2006). Biosorption characteristics of Bacillus sp. ATS-2 immobilized in silica gel for removal of Pb(II). J. Hazard. Mater.136 (2), 317323. 10.1016/j.jhazmat.2005.12.019

  • 41

    CamargoF. P.PradoP. F. D.TonelloP. S.Dos SantosA. C. A.DuarteI. C. S. (2018). Bioleaching of toxic metals from sewage sludge by co-inoculation of Acidithiobacillus and the biosurfactant-producing yeast Meyerozyma guilliermondii. J. Environ. Manage211, 2835. 10.1016/j.jenvman.2018.01.045

  • 42

    CameronH.MataM. T.RiquelmeC. (2018). The effect of heavy metals on the viability of Tetraselmis marina AC16-MESO and an evaluation of the potential use of this microalga in bioremediation. PeerJ6, e5295. 10.7717/peerj.5295

  • 43

    CepoiL.ZinicovscaiaI.ValutaA.CodreanuL.RudiL.ChiriacT.et al (2022). Bioremediation capacity of edaphic cyanobacteria Nostoc linckia for chromium in association with other heavy-metals-contaminated soils. Environ. - MDPI9 (1), 1. 10.3390/environments9010001

  • 44

    ChakrabortyR.AsthanaA.SinghA. K.JainB.SusanA. B. H. (2022). Adsorption of heavy metal ions by various low-cost adsorbents: a review. Int. J. Environ. Anal. Chem.102 (2), 342379. 10.1080/03067319.2020.1722811

  • 45

    ChamekhA.KharbechO.Driss-LimamR.FersiC.KhouatmeyaM.ChouariR. (2021). Evidences for antioxidant response and biosorption potential of Bacillus simplex strain 115 against lead. World J. Microbiol. Biotechnol.37 (3), 44. 10.1007/s11274-021-03009-2

  • 46

    ChangmaiM.PasawanM.PurkaitM. K. (2019). Treatment of oily wastewater from drilling site using electrocoagulation followed by microfiltration. Sep. Purif. Technol.210, 463472. 10.1016/j.seppur.2018.08.007

  • 47

    ChebotaryovaS. P.ZakharovaO. V.GusevA. A.BaranchikovP. A.KolesnikovE. A.YakushevaA. S.et al (2023). Assessment of the tolerance of a chlorophyte Desmodesmus to CuO-NP for evaluation of the nanopollution bioremediation potential of this microalga. Nanomater. (Basel)13 (4), 737. 10.3390/nano13040737

  • 48

    ChenB.LuoS.WuY.YeJ.WangQ.XuX.et al (2017). The effects of the endophytic bacterium Pseudomonas fluorescens Sasm05 and IAA on the plant growth and cadmium uptake of Sedum alfredii hance. Front. Microbiol.8 (DEC), 2538. 10.3389/fmicb.2017.02538

  • 49

    ChenL.ZhangX.ZhangM.ZhuY.ZhuoR. (2022). Removal of heavy-metal pollutants by white rot fungi: mechanisms, achievements, and perspectives. J. Clean. Prod.354, 131681. 10.1016/j.jclepro.2022.131681

  • 50

    ChenW.LiH. (2018). Cost-effectiveness analysis for soil heavy metal contamination treatments. Water, Air, Soil Pollut.229 (4), 126. 10.1007/s11270-018-3784-3

  • 51

    ChenY.HuK.ChenY. (2019). The effect of biotic and abiotic environmental factors on Pd(II) adsorption and reduction by Bacillus megaterium Y-4. Chemosphere220, 10581066. 10.1016/j.chemosphere.2019.01.011

  • 52

    ChenZ.HuangZ.ChengY.PanD.PanX.YuM.et al (2012). Cr(VI) uptake mechanism of Bacillus cereus. Chemosphere87 (3), 211216. 10.1016/j.chemosphere.2011.12.050

  • 53

    ChengJ.YinW.ChangZ.LundholmN.JiangZ. (2017). Biosorption capacity and kinetics of cadmium(II) on live and dead Chlorella vulgaris. J. Appl. Phycol.29 (1), 211221. 10.1007/s10811-016-0916-2

  • 54

    Concetta TomeiM.DaugulisA. J. (2013). Ex situ bioremediation of contaminated soils: an overview of conventional and innovative technologies. Crit. Rev. Environ. Sci. Technol.43 (20), 21072139. 10.1080/10643389.2012.672056

  • 55

    Corina-PetronelaM.TeodosiuC. (2007). Removal of persistent organic pollutants from textile wastewater by membrane processes. Environmental Engineering and Management Journal (EEMJ)6, 3.

  • 56

    CorsiI.Winther-NielsenM.SethiR.PuntaC.Della TorreC.LibralatoG.et al (2018). Ecofriendly nanotechnologies and nanomaterials for environmental applications: key issue and consensus recommendations for sustainable and ecosafe nanoremediation. Ecotoxicol. Environ. Saf.154, 237244. 10.1016/j.ecoenv.2018.02.037

  • 57

    DalCorsoG.FasaniE.ManaraA.VisioliG.FuriniA. (2019). Heavy metal pollution: state of the art and innovation in phytoremediation. Int. J. Mol. Sci.20 (14), 3412. 10.3390/ijms20143412

  • 58

    DaneshvarE.ZarrinmehrM. J.KoutraE.KornarosM.FarhadianO.BhatnagarA. (2019). Sequential cultivation of microalgae in raw and recycled dairy wastewater: microalgal growth, wastewater treatment and biochemical composition. Bioresour. Technol.273, 556564. 10.1016/j.biortech.2018.11.059

  • 59

    DasS.DasS.GhangrekarM. M. (2022). Efficacious bioremediation of heavy metals and radionuclides from wastewater employing aquatic macro- and microphytes. J. Basic Microbiol.62 (3-4), 260278. 10.1002/jobm.202100372

  • 60

    DashD. M.OsborneW. J. (2023). A systematic review on the implementation of advanced and evolutionary biotechnological tools for efficient bioremediation of organophosphorus pesticides. Chemosphere313, 137506. 10.1016/j.chemosphere.2022.137506

  • 61

    DashS.ChaudhuriH.GuptaR.NairU. G. (2018). Adsorption study of modified coal fly ash with sulfonic acid as a potential adsorbent for the removal of toxic reactive dyes from aqueous solution: kinetics and thermodynamics. J. Environ. Chem. Eng.6 (5), 58975905. 10.1016/j.jece.2018.05.017

  • 62

    da SilvaJ. R. R.GregorioA.Portela-CastroA. L. B.FernandesC. A. (2023) “Genotoxicity and cytotoxicity of textile production effluents, before and after Bacillus subitilis bioremediation, in Astyanax lacustris (Pisces, Characidae). Astyanax lacustris (Pisces, Characidae)886, 503588. 10.1016/j.mrgentox.2023.503588

  • 63

    Da SilvaL. I.PereiraM. C.de CarvalhoA. M. X.ButtrósV. H.PasqualM.DóriaJ. (2023). Phosphorus-solubilizing microorganisms: a key to sustainable agriculture. Agriculture13, 462. 10.3390/agriculture13020462

  • 64

    DaveP. N.ChopdaL. V. (2014). Application of iron oxide nanomaterials for the removal of heavy metals. J. Nanotechnol.2014, 114. 10.1155/2014/398569

  • 65

    DawwamG. E.AbdelfattahN. M.Abdel-MonemM. O.JahinH. S.OmerA. M.Abou-TalebK. A.et al (2023). An immobilized biosorbent from Paenibacillus dendritiformis dead cells and polyethersulfone for the sustainable bioremediation of lead from wastewater. Sci. Rep.13 (1), 891. 10.1038/s41598-023-27796-w

  • 66

    DehghaniM. H.KamalianS.ShayeghiM.YousefiM.HeidarinejadZ.AgarwalS.et al (2019). High-performance removal of diazinon pesticide from water using multi-walled carbon nanotubes. Microchemical Journal145, 486491.

  • 67

    Dell'AnnoF.Joaquim van ZylL.TrindadeM.BuschiE.CannavacciuoloA.PepiM.et al (2023). Microbiome enrichment from contaminated marine sediments unveils novel bacterial strains for petroleum hydrocarbon and heavy metal bioremediation. Environ. Pollut.317, 120772. 10.1016/j.envpol.2022.120772

  • 68

    Dell'AnnoF.RastelliE.BuschiE.BaroneG.BeolchiniF.Dell'AnnoA. (2022). Fungi can Be more effective than bacteria for the bioremediation of marine sediments highly contaminated with heavy metals. Microorganisms10 (5), 993. 10.3390/microorganisms10050993

  • 69

    Del Prado-AudeloM. L.García KerdanI.Escutia-GuadarramaL.Reyna-GonzálezJ. M.MagañaJ. J.Leyva-GómezG. (2021). Nanoremediation: nanomaterials and nanotechnologies for environmental cleanup. Front. Environ. Sci.9. 10.3389/fenvs.2021.793765

  • 70

    de Moura DickelJ. D.CarvalhoJ. K.SilveiraM. A. D.Menegotto Dos SantosP.RodriguesM. L. F.Fagundes-KlenM. R.et al (2022). Aspergillus sclerotiorum lipolytic activity and its application in bioremediation of high-fat dairy wastewater environments. Environ. Sci. Pollut. Res. Int.30, 3551735527. 10.1007/s11356-022-24669-z

  • 71

    Derakhshan NejadZ.JungM. C.KimK. H. (2018). Remediation of soils contaminated with heavy metals with an emphasis on immobilization technology. Environ. Geochem. Health40 (3), 927953. 10.1007/s10653-017-9964-z

  • 72

    DeviN. L. (2020). Persistent organic pollutants (POPs): environmental risks, toxicological effects, and bioremediation for environmental safety and challenges for future research. Singapore: Bioremediation of Industrial Waste for Environmental Safety, 5376.

  • 73

    DhaliwalS. S.SinghJ.TanejaP. K.MandalA. (2020). Remediation techniques for removal of heavy metals from the soil contaminated through different sources: a review. Environ. Sci. Pollut. Res.27 (2), 13191333. 10.1007/s11356-019-06967-1

  • 74

    DinM.NeloferR.SalmanM.KhanF. H.KhanA.AhmadM.et al (2019). Production of nitrogen fixing Azotobacter (SR-4) and phosphorus solubilizing Aspergillus Niger and their evaluation on Lagenaria siceraria and Abelmoschus esculentus. Biotechnol. Rep.22, e00323. 10.1016/j.btre.2019.e00323

  • 75

    DingC.ChenJ.ZhuF.ChaiL.LinZ.ZhangK.et al (2022). Biological toxicity of heavy metal(loid)s in natural environments: from microbes to humans. Front. Environ. Sci.10. 10.3389/fenvs.2022.920957

  • 76

    DubeyS.ChenC. W.HaldarD.TambatV. S.KumarP.TiwariA.et al (2023). Advancement in algal bioremediation for organic, inorganic, and emerging pollutants. Environ. Pollut.317, 120840. 10.1016/j.envpol.2022.120840

  • 77

    DwivediS. (2012). Bioremediation of heavy metal by algae: current and future perspective. J. Adv. Lab. Res. Biol.3 (3), 195199.

  • 78

    El-KhouryR.RakM.BénitP.JacobsH. T.RustinP. (2022). Cyanide resistant respiration and the alternative oxidase pathway: a journey from plants to mammals. Biochimica Biophysica Acta - Bioenergetics1863 (6), 148567. 10.1016/j.bbabio.2022.148567

  • 79

    EpeldeL.BurgesA.MijangosI.GarbisuC. (2014). Microbial properties and attributes of ecological relevance for soil quality monitoring during a chemical stabilization field study. Appl. Soil Ecol.75, 112. 10.1016/j.apsoil.2013.10.003

  • 80

    EtemadiM.SamadiS.YazdS. S.JafariP.YousefiN.AliabadiM. (2017). Selective adsorption of Cr(VI) ions from aqueous solutions using Cr6+-imprinted Pebax/chitosan/GO/APTES nanofibrous adsorbent. Int. J. Biol. Macromol.95, 725733. 10.1016/j.ijbiomac.2016.11.117

  • 81

    EyankwareM. O.ObasiP. N. (2021). A holistic review of heavy metals in water and soil in Ebonyi SE. Nigeria; with emphasis on its effects on human, aquatic organisms and plants. World News Nat. Sci.38, 119.

  • 82

    FatoF. P.LiD. W.ZhaoL. J.QiuK.LongY. T. (2019). Simultaneous removal of multiple heavy metal ions from river water using ultrafine mesoporous magnetite nanoparticles. ACS Omega4 (4), 75437549. 10.1021/acsomega.9b00731

  • 83

    FeiL.BilalM.QamarS. A.ImranH. M.RiasatA.JahangeerM.et al (2022). Nano-remediation technologies for the sustainable mitigation of persistent organic pollutants. Environ. Res.211, 113060. 10.1016/j.envres.2022.113060

  • 84

    FengJ. R.DengQ. X.HanS. K.NiH. G. (2023). Use of nanoparticle-coated bacteria for the bioremediation of organic pollution: a mini review. Chemosphere313, 137391. 10.1016/j.chemosphere.2022.137391

  • 85

    FengL.YanH.DaiC.XuW.GuF.ZhangF.et al (2020). The systematic exploration of cadmium-accumulation characteristics of maize kernel in acidic soil with different pollution levels in China. Sci. Total Environ.729, 138972. 10.1016/j.scitotenv.2020.138972

  • 86

    FulekarM. H.SharmaJ.TendulkarA. (2012). Bioremediation of heavy metals using biostimulation in laboratory bioreactor. Environ. Monit. Assess.184 (12), 72997307. 10.1007/s10661-011-2499-3

  • 87

    FuntikovaT. V.AkhmetovL. I.PuntusI. F.MikhailovP. A.AppazovN. O.NarmanovaR. A.et al (2023). Bioremediation of oil-contaminated soil of the republic of Kazakhstan using a new biopreparation. Microorganisms11 (2), 522. 10.3390/microorganisms11020522

  • 88

    FurnholmT.RehanM.WishartJ.TisaL. S. J. M. (2017). Pb2+ tolerance by Frankia sp. strain EAN1pec involves surface-binding. , 163(4), 472487. 10.1099/mic.0.000439

  • 89

    GabrR. M.HassanS. H. A.ShoreitA. A. M. (2008). Biosorption of lead and nickel by living and non-living cells of Pseudomonas aeruginosa ASU 6a. Int. Biodeterior. Biodegrad.62 (2), 195203. 10.1016/j.ibiod.2008.01.008

  • 90

    GaurN.FloraG.YadavM.TiwariA. (2014). A review with recent advancements on bioremediation-based abolition of heavy metals. Environ. Sci. Process Impacts16 (2), 180193. 10.1039/c3em00491k

  • 91

    GavrilescuM. (2022). Enhancing phytoremediation of soils polluted with heavy metals. Curr. Opin. Biotechnol.74, 2131. 10.1016/j.copbio.2021.10.024

  • 92

    GentryT. J.RensingC.PepperI. L. (2004). New approaches for bioaugmentation as a remediation technology. Crit. Rev. Environ. Sci. Technol.34 (5), 447494. 10.1080/10643380490452362

  • 93

    GoherM. E.El-MonemA. M. A.Abdel-SatarA. M.AliM. H.HussianA. E. M.Napiórkowska-KrzebietkeA.et al (2016). Biosorption of some toxic metals from aqueous solution using non-living algal cells of Chlorella vulgaris. J. Elem.21 (3), 703714. 10.5601/jelem.2015.20.4.1037

  • 94

    GongY.ZhaoD.WangQ. (2018). An overview of field-scale studies on remediation of soil contaminated with heavy metals and metalloids: technical progress over the last decade. Water Res.147, 440460. 10.1016/j.watres.2018.10.024

  • 95

    González-ChávezM. C.Carrillo-GonzálezR.WrightS. F.NicholsK. A. (2004). The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ. Pollut.130 (3), 317323. 10.1016/j.envpol.2004.01.004

  • 96

    GoswamiR. K.AgrawalK.ShahM. P.VermaP. (2022). Bioremediation of heavy metals from wastewater: a current perspective on microalgae-based future. Lett. Appl. Microbiol.75 (4), 701717. 10.1111/lam.13564

  • 97

    GrimmF. A.KlarenW. D.LiX.LehmlerH. J.KarmakarM.RobertsonL. W.et al (2020). Cardiovascular effects of polychlorinated biphenyls and their major metabolites. Environ. Health Perspect.128 (7), 7700877013. 10.1289/EHP7030

  • 98

    GulzarA. B. M.MazumderP. B. (2022). Helping plants to deal with heavy metal stress: the role of nanotechnology and plant growth promoting rhizobacteria in the process of phytoremediation. Environ. Sci. Pollut. Res.29 (27), 4031940341. 10.1007/s11356-022-19756-0

  • 99

    GuoW.PanB.SakkiahS.YavasG.GeW.ZouW.et al (2019). Persistent organic pollutants in food: contamination sources, health effects and detection methods. Int. J. Environ. Res. Public Health16 (22), 4361. 10.3390/ijerph16224361

  • 100

    GururaniM. A.UpadhyayaC. P.BaskarV.VenkateshJ.NookarajuA.ParkS. W. (2013). Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. J. Plant Growth Regul.32 (2), 245258. 10.1007/s00344-012-9292-6

  • 101

    HananingtyasI.NuryantyC. D.KarlinasariL.AlikodraH. S.JayanegaraA.SumantriA. (2022). The effects of heavy metal exposure in agriculture soil on chlorophyll content of agriculture crops: a meta-analysis approach. IOP Conf. Ser. Earth Environ. Sci.951, 012044. Paper presented at the. 10.1088/1755-1315/951/1/012044

  • 102

    HanifA.BhattiH. N.HanifM. A. (2015). Removal of zirconium from aqueous solution by Ganoderma lucidum: biosorption and bioremediation studies. Desalination Water Treat.53 (1), 195205. 10.1080/19443994.2013.837005

  • 103

    HemlataMeenaP. R.SinghA. P.TejavathK. K. (2020). Biosynthesis of silver nanoparticles using cucumis prophetarum aqueous leaf extract and their antibacterial and antiproliferative activity against cancer cell lines. ACS Omega5 (10), 55205528. 10.1021/acsomega.0c00155

  • 104

    HlihorR. M.RoscaM.Hagiu-ZaleschiL.SimionI. M.DarabanG. M.StoleruV. (2022). Medicinal plant growth in heavy metals contaminated soils: responses to metal stress and induced risks to human health. Toxics10 (9), 499. 10.3390/toxics10090499

  • 105

    HotaS.SharmaG. K.SubrahmanyamG.KumarA.ShabnamA. A.BaruahP.et al (2021). Fungal communities for bioremediation of contaminated soil for sustainable environments. Recent Trends Mycol. Res. Environ. Industrial Perspective2, 2742. 10.1007/978-3-030-68260-6_2

  • 106

    HouriT.KhairallahY.ZahabA. A.OstaB.RomanosD.HaddadG. (2020). Heavy metals accumulation effects on the photosynthetic performance of geophytes in mediterranean reserve. J. King Saud Univ. - Sci.32 (1), 874880. 10.1016/j.jksus.2019.04.005

  • 107

    HuX.WangJ.LvY.LiuX.ZhongJ.CuiX.et al (2021). Effects of heavy metals/metalloids and soil properties on microbial communities in farmland in the vicinity of a metals smelter. Front. Microbiol.12, 707786. 10.3389/fmicb.2021.707786

  • 108

    HuangC. C.LiangC. M.YangT. I.ChenJ. L.WangW. K. (2021). Shift of bacterial communities in heavy metal-contaminated agricultural land during a remediation process. PLoS ONE16 (7 July), e0255137. 10.1371/journal.pone.0255137

  • 109

    HuangF.ZhouH.GuJ.LiuC.YangW.LiaoB.et al (2020). Differences in absorption of cadmium and lead among fourteen sweet potato cultivars and health risk assessment. Ecotoxicol. Environ. Saf.203, 111012. 10.1016/j.ecoenv.2020.111012

  • 110

    HuangL.NiJ.ZhongC.XuP.DaiJ.TangH. (2022). Establishment of a salt-induced bioremediation platform from marine Vibrio natriegens. Commun. Biol.5 (1), 1352. 10.1038/s42003-022-04319-3

  • 111

    HuangL.WangW.ZanaroliG.XuP.TangH. (2021). Hexabromocyclododecanes are dehalogenated by CYP168A1 from Pseudomonas aeruginosa strain HS9. Appl. Environ. Microbiol.87 (17), 00826211e82711. 10.1128/AEM.00826-21

  • 112

    HubeS.EskafiM.HrafnkelsdóttirK. F.BjarnadóttirB.BjarnadóttirM. Á.AxelsdóttirS.et al (2020). Direct membrane filtration for wastewater treatment and resource recovery: a review. Sci. Total Environ.710, 136375. 10.1016/j.scitotenv.2019.136375

  • 113

    HusainR.VikramN.YadavG.KumarD.PandeyS.PatelM.et al (2022). “Microbial bioremediation of heavy metals by Marine bacteria,” in Development in wastewater treatment research and processes: microbial degradation of xenobiotics through bacterial and fungal approach, 177203.

  • 114

    ImronM. F.KurniawanS. B.AbdullahS. R. S. (2021). Resistance of bacteria isolated from leachate to heavy metals and the removal of Hg by Pseudomonas aeruginosa strain FZ-2 at different salinity levels in a batch biosorption system. Sustain. Environ. Res.31 (1), 14. 10.1186/s42834-021-00088-6

  • 115

    IzanlooM.MehrpooyaM.DelpishehM. (2021). Integrated thermochemical Mg‐Cl‐Na hydrogen production cycle, carbon dioxide capture, ammonia production, and methanation. International Journal of Energy Research45 (7), 1071910737.

  • 116

    IslamM. N.TakiG.NguyenX. P.JoY. T.KimJ.ParkJ. H. (2017). Heavy metal stabilization in contaminated soil by treatment with calcined cockle shell. Environ. Sci. Pollut. Res.24 (8), 71777183. 10.1007/s11356-016-8330-5

  • 117

    JabbarN. M.AlardhiS. M.MohammedA. K.SalihI. K.AlbayatiT. M. (2022). Challenges in the implementation of bioremediation processes in petroleum-contaminated soils: a review. Environ. Nanotechnol. Monit. Manag.18, 100694. 10.1016/j.enmm.2022.100694

  • 118

    JiaW.LiN.YangT.DaiW.JiangJ.ChenK.et al (2021). Bioaugmentation of atrazine-contaminated soil with paenarthrobacter sp. strain AT-5 and its effect on the soil microbiome. Front. Microbiol.12, 771463. 10.3389/fmicb.2021.771463

  • 119

    JiaY.LiaoZ.ChewH.WangL.LinB.ChenC.et al (2020). Effect of Pennisetum giganteum z.x. lin mixed nitrogen-fixing bacterial fertilizer on the growth, quality, soil fertility and bacterial community of pakchoi (Brassica chinensis L.). PLoS ONE15, e0228709. 10.1371/journal.pone.0228709

  • 120

    JiaZ.LiS.WangL. (2018). Assessment of soil heavy metals for eco-environment and human health in a rapidly urbanization area of the upper Yangtze Basin. Sci. Rep.8 (1), 3256. 10.1038/s41598-018-21569-6

  • 121

    KadamA.SarataleR. G.ShindeS.YangJ.HwangK.MistryB.et al (2019). Adsorptive remediation of cobalt oxide nanoparticles by magnetized α-cellulose fibers from waste paper biomass. Bioresour. Technol.273, 386393. 10.1016/j.biortech.2018.11.041

  • 122

    KalaivananD.GaneshamurthyA. N. (2016). “Mechanisms of heavy metal toxicity in plants,” in Abiotic stress physiology of horticultural crops, 85102.

  • 123

    KamikaI.MombaM. N. (2013). Assessing the resistance and bioremediation ability of selected bacterial and protozoan species to heavy metals in metal-rich industrial wastewater. BMC Microbiol.13, 28. 10.1186/1471-2180-13-28

  • 124

    Karimi-ShamsabadiM.Nezamzadeh-EjhiehA. (2016). Comparative study on the increased photoactivity of coupled and supported manganese-silver oxides onto a natural zeolite nano-particles. Journal of Molecular Catalysis A: Chemical418, 103114.

  • 125

    KashemA. H. M.DasP.AbdulQuadirM.KhanS.ThaherM. I.AlghasalG.et al (2023). Microalgal bioremediation of brackish aquaculture wastewater. Sci. Total Environ.873, 162384. 10.1016/j.scitotenv.2023.162384

  • 126

    KaushikS.AlatawiA.DjiwantiS. R.PandeA.SkottiE.SoniV. (2021). Potential of extremophiles for bioremediation. Microb. Rejuvenation Polluted Environ.1, 293328. 10.1007/978-981-15-7447-4_12

  • 127

    KhanA. A.JilaniG.AkhtarM. S.NaqviS. M. S.RasheedM. (2009). Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. J. Agric. Biol. Sci.1 (1), 4858.

  • 128

    KhanA. L.WaqasM.HussainJ.Al-HarrasiA.LeeI. J. (2014). Fungal endophyte Penicillium janthinellum LK5 can reduce cadmium toxicity in Solanum lycopersicum (Sitiens and Rhe). Biol. Fertil. Soils50 (1), 7585. 10.1007/s00374-013-0833-3

  • 129

    KhanS. H.PathakB.FulekarM. H. (2018). Synthesis, characterization and photocatalytic degradation of chlorpyrifos by novel Fe: ZnO nanocomposite material. Nanotechnology for Environmental Engineering3, 114.

  • 130

    KimB. K.ParkG. Y.JeonE. K.JungJ. M.JungH. B.KoS. H.et al (2013). Field application of in situ electrokinetic remediation for as-Cu-and Pb-contaminated paddy soil. Water, Air, Soil Pollut.224 (9), 1698. 10.1007/s11270-013-1698-7

  • 131

    KimH. W.SeokY. S.ChoT. J.RheeM. S. (2020). Risk factors influencing contamination of customized cosmetics made on-the-spot: evidence from the national pilot project for public health. Sci. Rep.10 (1), 1561. 10.1038/s41598-020-57978-9

  • 132

    KrithikaS.BalachandarD. (2016). Expression of zinc transporter genes in rice as influenced by zinc-solubilizing enterobacter cloacae strain ZSB14. Front. Plant Sci.7 (APR2016), 446. 10.3389/fpls.2016.00446

  • 133

    KuanK. B.OthmanR.RahimK. A.ShamsuddinZ. H. (2016). Plant growth-promoting rhizobacteria inoculation to enhance vegetative growth, nitrogen fixation and nitrogen remobilisation of maize under greenhouse conditions. PLoS ONE11 (3), e0152478. 10.1371/journal.pone.0152478

  • 134

    KumarH.IshtiyaqS.VarunM.FavasP. J. C.OgunkunleC. O.PaulM. S. (2022). Bioremediation: plants and microbes for restoration of heavy metal contaminated soils. Bioenergy Crops3, 3770. 10.1201/9781003043522-3

  • 135

    KumarH.SinhaS. K.GoudV. V.DasS. (2019). Removal of Cr(VI) by magnetic iron oxide nanoparticles synthesized from extracellular polymeric substances of chromium resistant acid-tolerant bacterium Lysinibacillus sphaericus RTA-01. J. Environ. Health Sci. Eng.17 (2), 10011016. 10.1007/s40201-019-00415-5

  • 136

    KumarK.SinghD. (2023). Toxicity and bioremediation of the lead: a critical review. Int. J. Environ. Health Res.34, 18791909. 10.1080/09603123.2023.2165047

  • 137

    KumarS.SaxenaS. (2019). Arbuscular mycorrhizal fungi (AMF) from heavy metal-contaminated soils: molecular approach and application in phytoremediation. Biofertilizers Sustain. Agric. Environ., 489500. 10.1007/978-3-030-18933-4_22

  • 138

    KumarV.DwivediS. K. (2021). Bioremediation mechanism and potential of copper by actively growing fungus Trichoderma lixii CR700 isolated from electroplating wastewater. J. Environ. Manag.277, 111370. 10.1016/j.jenvman.2020.111370

  • 139

    KumarV.KumarH.VishalV.LalS. (2023). Studies on the morphology, phylogeny, and bioremediation potential of Penicillium citrinum and Paecilomyces variotii (Eurotiales) from oil-contaminated areas. Arch. Microbiol.205 (1), 50. 10.1007/s00203-022-03383-x

  • 140

    KurniawanS. B.RamliN. N.SaidN. S. M.AliasJ.ImronM. F.AbdullahS. R. S.et al (2022). Practical limitations of bioaugmentation in treating heavy metal contaminated soil and role of plant growth promoting bacteria in phytoremediation as a promising alternative approach. Heliyon8 (4), e08995. 10.1016/j.heliyon.2022.e08995

  • 141

    LambertM.LevenB. A.GreenR. M. (2000). New methods of cleaning up heavy metal in soils and water. Environ. Sci. Technol. Briefs Citizens, 13.

  • 142

    Landa‐fazA.González‐orengaS.BoscaiuM.Rodríguez‐vázquezR.VicenteO. (2021). Effect of the pesticide endosulfan and two different biostimulants on the stress responses of phaseolus leptostachyus plants grown in a saline soil. Agronomy11 (6), 1208. 10.3390/agronomy11061208

  • 143

    LeeD. W.LeeH.KwonB. O.KhimJ. S.YimU. H.KimB. S.et al (2018). Biosurfactant-assisted bioremediation of crude oil by indigenous bacteria isolated from Taean beach sediment. Environ. Pollut.241, 254264. 10.1016/j.envpol.2018.05.070

  • 144

    LeeJ.KimJ.AhmedS. R.ZhouH.KimJ. M.LeeJ. (2014). Plasmon-induced photoluminescence immunoassay for tuberculosis monitoring using gold-nanoparticle-decorated graphene. ACS Appl. Mater. Interfaces6 (23), 2138021388. 10.1021/am506389m

  • 145

    Leon-VazA.LeonR.GiraldezI.VegaJ. M.VigaraJ. (2021). Impact of heavy metals in the microalga Chlorella sorokiniana and assessment of its potential use in cadmium bioremediation. Aquat. Toxicol.239, 105941. 10.1016/j.aquatox.2021.105941

  • 146

    LiD.ZhengX.LinL.AnQ.JiaoY.LiQ.et al (2022). Remediation of soils co-contaminated with cadmium and dichlorodiphenyltrichloroethanes by king grass associated with Piriformospora indica: insights into the regulation of root excretion and reshaping of rhizosphere microbial community structure. J. Hazard. Mater.422, 126936. 10.1016/j.jhazmat.2021.126936

  • 147

    LiQ.ZhongH.CaoY. (2020). Effective extraction and recovery of rare earth elements (REEs) in contaminated soils using a reusable biosurfactant. Chemosphere256, 127070. 10.1016/j.chemosphere.2020.127070

  • 148

    LiW.ChenY.WangT. (2021). Cadmium biosorption by lactic acid bacteria Weissella viridescens ZY-6. Food control.123, 107747. 10.1016/j.foodcont.2020.107747

  • 149

    LiZ.HeY.SonneC.LamS. S.KirkhamM. B.BolanN.et al (2023). A strategy for bioremediation of nuclear contaminants in the environment. Environ. Pollut.319, 120964. 10.1016/j.envpol.2022.120964

  • 150

    LiaqatI.MuhammadN.AraC.HanifU.AndleebS.ArshadM.et al (2023). Bioremediation of heavy metals polluted environment and decolourization of black liquor using microbial biofilms. Mol. Biol. Rep.50, 39853997. 10.1007/s11033-023-08334-3

  • 151

    LinJ.JiangW.LiuD. (2003). Accumulation of copper by roots, hypocotyls, cotyledons and leaves of sunflower (Helianthus annuus L.). Bioresour. Technol.86 (2), 151155. 10.1016/S0960-8524(02)00152-9

  • 152

    LiuH.GuoS.JiaoK.HouJ.XieH.XuH. (2015). Bioremediation of soils co-contaminated with heavy metals and 2,4,5-trichlorophenol by fruiting body of Clitocybe maxima. J. Hazard Mater294, 121127. 10.1016/j.jhazmat.2015.04.004

  • 153

    LiuJ.QiW.LiQ.WangS.-G.SongC.YuanX.-z. (2020). Exogenous phosphorus-solubilizing bacteria changed the rhizosphere microbial community indirectly. 3 Biotech.10, 164211. 10.1007/s13205-020-2099-4

  • 154

    LiuS.ZhengY.MaY.SarwarA.ZhaoX.LuoT.et al (2019a). Evaluation and proteomic analysis of lead adsorption by lactic acid bacteria. Int. J. Mol. Sci.20 (22), 5540. 10.3390/ijms20225540

  • 155

    LiuS. H.ZengG. M.NiuQ. Y.LiuY.ZhouL.JiangL. H.et al (2017). Bioremediation mechanisms of combined pollution of PAHs and heavy metals by bacteria and fungi: a mini review. Bioresour. Technol.224, 2533. 10.1016/j.biortech.2016.11.095

  • 156

    LiuW.ZuoQ.ZhaoC.WangS.ShiY.LiangS.et al (2018). Effects of Bacillus subtilis and nanohydroxyapatite on the metal accumulation and microbial diversity of rapeseed (Brassica campestris L.) for the remediation of cadmium-contaminated soil. Environ. Sci. Pollut. Res.25 (25), 2521725226. 10.1007/s11356-018-2616-8

  • 157

    LiuZ.LuB.XiaoH.LiuD.LiX.WangL. A.et al (2019b). Effect of mixed solutions of heavy metal eluents on soil fertility and microorganisms. Environ. Pollut.254, 112968. 10.1016/j.envpol.2019.112968

  • 158

    LuM.JiaoS.GaoE.SongX.LiZ.HaoX.et al (2017). Transcriptome response to heavy metals in sinorhizobium meliloti CCNWSX0020 reveals new metal resistance determinants that also promote bioremediation by Medicago lupulina in metal-contaminated soil. Appl. Environ. Microbiol.83 (20), e01244. 10.1128/AEM.01244-17

  • 159

    LuP.LiQ.LiuH.FengZ.YanX.HongQ.et al (2013). Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by Cupriavidus sp. DT-1. Bioresour. Technol.127, 337342. 10.1016/j.biortech.2012.09.116

  • 160

    LuoH.WangQ.LiuZ.WangS.LongA.YangY. (2020a). Potential bioremediation effects of seaweed Gracilaria lemaneiformis on heavy metals in coastal sediment from a typical mariculture zone. Chemosphere245, 125636. 10.1016/j.chemosphere.2019.125636

  • 161

    LuoJ.DengJ.CuiL.ChangP.DaiX.YangC.et al (2020b). The potential assessment of green alga Chlamydomonas reinhardtii CC-503 in the biodegradation of benz(a)anthracene and the related mechanism analysis. Chemosphere249, 126097. 10.1016/j.chemosphere.2020.126097

  • 162

    LwinH. M.ZhanW.SongS.JiaF.ZhouJ. (2019). Visible-light photocatalytic degradation pathway of tetracycline hydrochloride with cubic structured ZnO/SnO2 heterojunction nanocatalyst. Chem. Phys. Lett.736, 136806. 10.1016/j.cplett.2019.136806

  • 163

    MaX. K.LiT. T.FamH.Charles PetersonE.ZhaoW. W.GuoW.et al (2018). The influence of heavy metals on the bioremediation of polycyclic aromatic hydrocarbons in aquatic system by a bacterial-fungal consortium. Environ. Technol.39 (16), 21282137. 10.1080/09593330.2017.1351492

  • 164

    MahdaviV.TaghadosiF.DashtestaniF.BahadorikhaliliS.FarimaniM. M.FarimaniL.et al (2021). Aminoguanidine modified magnetic graphene oxide as a robust nanoadsorbent for efficient removal and extraction of chlorpyrifos residue from water. Journal of Environmental Chemical Engineering9 (5), 106117

  • 165

    MalikS.KishoreS.ShahM. P.KumarS. A. (2022). A comprehensive review on nanobiotechnology for bioremediation of heavy metals from wastewater. J. Basic Microbiol.62 (3-4), 361375. 10.1002/jobm.202100555

  • 166

    ManobalaT.ShuklaS. K.RaoT. S.KumarM. D. (2021). Kinetic modelling of the uranium biosorption by Deinococcus radiodurans biofilm. Chemosphere269, 128722. 10.1016/j.chemosphere.2020.128722

  • 167

    ManojS. R.KarthikC.KadirveluK.ArulselviP. I.ShanmugasundaramT.BrunoB.et al (2020). Understanding the molecular mechanisms for the enhanced phytoremediation of heavy metals through plant growth promoting rhizobacteria: a review. J. Environ. Manag.254, 109779. 10.1016/j.jenvman.2019.109779

  • 168

    ManzoorN.AhmedT.NomanM.ShahidM.NazirM. M.AliL.et al (2021). Iron oxide nanoparticles ameliorated the cadmium and salinity stresses in wheat plants, facilitating photosynthetic pigments and restricting cadmium uptake. Sci. Total Environ.769, 145221. 10.1016/j.scitotenv.2021.145221

  • 169

    MaoC.SongY.ChenL.JiJ.LiJ.YuanX.et al (2019). Human health risks of heavy metals in paddy rice based on transfer characteristics of heavy metals from soil to rice. Catena175, 339348. 10.1016/j.catena.2018.12.029

  • 170

    MaoJ.GuanW. (2016). Fungal degradation of polycyclic aromatic hydrocarbons (PAHs) by Scopulariopsis brevicaulis and its application in bioremediation of PAH-contaminated soil. Acta Agric. Scand. Sect. B Soil Plant Sci.66 (5), 399405. 10.1080/09064710.2015.1137629

  • 171

    MasottiF.GaravagliaB. S.GottigN.OttadoJ. (2023). Bioremediation of the herbicide glyphosate in polluted soils by plant-associated microbes. Curr. Opin. Microbiol.73, 102290. 10.1016/j.mib.2023.102290

  • 172

    MathivananK.ChandirikaJ. U.MathimaniT.RajaramR.AnnaduraiG.YinH. (2021a). Production and functionality of exopolysaccharides in bacteria exposed to a toxic metal environment. Ecotoxicol. Environ. Saf.208, 111567. 10.1016/j.ecoenv.2020.111567

  • 173

    MathivananK.ChandirikaJ. U.VinothkannaA.YinH.LiuX.MengD. (2021b). Bacterial adaptive strategies to cope with metal toxicity in the contaminated environment – a review. Ecotoxicol. Environ. Saf.226, 112863. 10.1016/j.ecoenv.2021.112863

  • 174

    MazumderA.BhattacharyaS.BhattacharjeeC. (2020). Role of nano-photocatalysis in heavy metal detoxification. Nanophotocatalysis Environ. Appl., 133. 10.1007/978-3-030-12619-3_1

  • 175

    McGrathS. P.ZhaoF. J.LombiE. (2001). Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil232 (1-2), 207214. 10.1023/A:1010358708525

  • 176

    MitraS.ChakrabortyA. J.TareqA. M.EmranT. B.NainuF.KhusroA.et al (2022). Impact of heavy metals on the environment and human health: novel therapeutic insights to counter the toxicity. J. King Saud Univ. - Sci.34 (3), 101865. 10.1016/j.jksus.2022.101865

  • 177

    MohammadiA.VeisiP. (2018). High adsorption performance of β-cyclodextrin-functionalized multi-walled carbon nanotubes for the removal of organic dyes from water and industrial wastewater. Journal of Environmental Chemical Engineering6 (4), 46344643.

  • 178

    MonacheseM.BurtonJ. P.ReidG. (2012). Bioremediation and tolerance of humans to heavy metals through microbial processes: a potential role for probiotics?Appl. Environ. Microbiol.78 (18), 63976404. 10.1128/AEM.01665-12

  • 179

    MoreT. T.YadavJ. S. S.YanS.TyagiR. D.SurampalliR. Y. (2014). Extracellular polymeric substances of bacteria and their potential environmental applications. J. Environ. Manag.144, 125. 10.1016/j.jenvman.2014.05.010

  • 180

    MustaphaM. U.HalimoonN. (2022). The effect of heavy metals on biodegradation of carbofuran by microbial strain enriched from agricultural areas. Afr. J. Biol. Sci.18, 7177. 10.21608/ajbs.2022.251286

  • 181

    NagashettiV.MahadevarajuG. K.MuralidharT. S.JavedA.TrivediD.BhusalK. P. (2013). Biosorption of heavy metals from soil by Pseudomonas aeruginosa. Int. J. Innovative Technol. Explor. Eng.2 (6), 2224.

  • 182

    NandiniR.AmuthavallinayakiM.SangameswaranR.ArtheR. (2023). A review on nano enhanced bioremediation of toxic contaminants in the environment. Int. J. Mod. Dev. Eng. Sci.2 (6), 2834.

  • 183

    NathD.MauryaB. R.MeenaV. S. (2017). Documentation of five potassium-and phosphorus-solubilizing bacteria for their K and P-solubilization ability from various minerals. Biocatal. Agric. Biotechnol.10, 174181. 10.1016/j.bcab.2017.03.007

  • 184

    NawazH.Anwar-ul-HaqM.AkhtarJ.ArfanM. (2021). Cadmium, chromium, nickel and nitrate accumulation in wheat (Triticum aestivum L.) using wastewater irrigation and health risks assessment. Ecotoxicol. Environ. Saf.208, 111685. 10.1016/j.ecoenv.2020.111685

  • 185

    NedjimiB. (2021). Phytoremediation: a sustainable environmental technology for heavy metals decontamination. SN Appl. Sci.3 (3), 286. 10.1007/s42452-021-04301-4

  • 186

    NeeliS. T.RamsurnH.NgC. Y.WangY.LuJ. (2020). Removal of Cr (VI), as (V), Cu (II), and Pb (II) using cellulose biochar supported iron nanoparticles: a kinetic and mechanistic study. J. Environ. Chem. Eng.8 (5), 103886. 10.1016/j.jece.2020.103886

  • 187

    NomanM.AhmedT.HussainS.NiaziM. B. K.ShahidM.SongF. (2020). Biogenic copper nanoparticles synthesized by using a copper-resistant strain Shigella flexneri SNT22 reduced the translocation of cadmium from soil to wheat plants. J. Hazard. Mater.398, 123175. 10.1016/j.jhazmat.2020.123175

  • 188

    Oatley-RadcliffeD. L.BarronA. R. (2022). “Summary of field trial results of the treatment of contaminated water using non-fouling super hydrophilic functionalized ceramic membranes,” in Sustainable Energy-Water-Environment Nexus in Deserts: Proceeding of the First International Conference on Sustainable Energy-Water-Environment Nexus in Desert ClimatesCham: Springer International Publishing, 22948121129.

  • 189

    O'ConnellD. W.BirkinshawC.O'DwyerT. F. (2008). Heavy metal adsorbents prepared from the modification of cellulose: a review. Bioresour. Technol.99 (15), 67096724. 10.1016/j.biortech.2008.01.036

  • 190

    OjuederieO. B.BabalolaO. O. (2017). Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int. J. Environ. Res. Public Health14 (12), 1504. 10.3390/ijerph14121504

  • 191

    OladoyeP. O.OloweO. M.AsemoloyeM. D. (2022). Phytoremediation technology and food security impacts of heavy metal contaminated soils: a review of literature. Chemosphere288, 132555. 10.1016/j.chemosphere.2021.132555

  • 192

    O'NeilR. A.HolmesD. E.CoppiM. V.AdamsL. A.LarrahondoM. J.WardJ. E.et al (2008). Gene transcript analysis of assimilatory iron limitation in Geobacteraceae during groundwater bioremediation. Environ. Microbiol.10 (5), 12181230. 10.1111/j.1462-2920.2007.01537.x

  • 193

    OrdookhaniK.KhavaziK.MoezziA.RejaliF. (2010). Influence of PGPR and AMF on antioxidant activity, lycopene and potassium contents in tomato. Afr. J. Agric. Res.5 (10), 11081116.

  • 194

    PachaiappanR.RajendranS.ShowP. L.ManavalanK.NaushadM. (2021). Metal/metal oxide nanocomposites for bactericidal effect: a review. Chemosphere272, 128607. 10.1016/j.chemosphere.2020.128607

  • 195

    PalanivelT. M.PracejusB.NovoL. A. B. (2023). Bioremediation of copper using indigenous fungi Aspergillus species isolated from an abandoned copper mine soil. Chemosphere314, 137688. 10.1016/j.chemosphere.2022.137688

  • 196

    PandeV.PandeyS. C.SatiD.BhattP.SamantM. (2022). Microbial interventions in bioremediation of heavy metal contaminants in agroecosystem. Front. Microbiol.6 (13), 824084. 10.3389/fmicb.2022.824084

  • 197

    PangY.ZengG. M.TangL.ZhangY.LiuY. Y.LeiX. X.et al (2011). Cr(VI) reduction by Pseudomonas aeruginosa immobilized in a polyvinyl alcohol/sodium alginate matrix containing multi-walled carbon nanotubes. Bioresour. Technol.102 (22), 1073310736. 10.1016/j.biortech.2011.08.078

  • 198

    ParkB.SonY. (2017). Ultrasonic and mechanical soil washing processes for the removal of heavy metals from soils. Ultrason. Sonochemistry35, 640645. 10.1016/j.ultsonch.2016.02.002

  • 199

    PathaniaP.BhatiaR.KhatriM. (2020). Cross-competence and affectivity of maize rhizosphere bacteria Bacillus sp. MT7 in tomato rhizosphere. Sci. Hortic.272, 109480. 10.1016/j.scienta.2020.109480

  • 200

    PereraI. C.HemamaliE. H. (2022). Genetically modified organisms for bioremediation: current research and advancements. Bioremediation Environ. Pollut. Emerg. Trends Strategies, 163186. 10.1007/978-3-030-86169-8_7

  • 201

    Pinel-CabelloM.JaureguiR.JroundiF.GeffersR.JarekM.LinkA.et al (2023). Genetic mechanisms for Se(VI) reduction and synthesis of trigonal 1-D nanostructures in Stenotrophomonas bentonitica: perspectives in eco-friendly nanomaterial production and bioremediation. Sci. Total Environ.862, 160635. 10.1016/j.scitotenv.2022.160635

  • 202

    PriyadarshaneeM.DasS. (2021). Biosorption and removal of toxic heavy metals by metal tolerating bacteria for bioremediation of metal contamination: a comprehensive review. J. Environ. Chem. Eng.9 (1), 104686. 10.1016/j.jece.2020.104686

  • 203

    PunethaA.SaraswatS.RaiJ. P. N. (2022). An insight on microbial degradation of benzo[a]pyrene: current status and advances in research. World J. Microbiol. Biotechnol.38 (4), 61. 10.1007/s11274-022-03250-3

  • 204

    RahmanZ.SinghV. P. (2020). Bioremediation of toxic heavy metals (THMs) contaminated sites: concepts, applications and challenges. Environ. Sci. Pollut. Res. Int.27 (22), 2756327581. 10.1007/s11356-020-08903-0

  • 205

    RaniA.SoucheY. S.GoelR. (2009). Comparative assessment of in situ bioremediation potential of cadmium resistant acidophilic Pseudomonas putida 62BN and alkalophilic Pseudomonas monteilli 97AN strains on soybean. Int. Biodeterior. Biodegrad.63 (1), 6266. 10.1016/j.ibiod.2008.07.002

  • 206

    RavindraK.MorS. (2019). Distribution and health risk assessment of arsenic and selected heavy metals in Groundwater of Chandigarh, India. Environ. Pollut.250, 820830. 10.1016/j.envpol.2019.03.080

  • 207

    ReddyK. R.ParupudiU. S. (1997). Removal of chromium, nickel and cadmium from clays by in-situ electrokinetic remediation. Soil Sediment Contam.6 (4), 391407. 10.1080/15320389709383574

  • 208

    RiazM.KamranM.FangY.WangQ.CaoH.YangG.et al (2021). Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: a critical review. J. Hazard. Mater.402, 123919. 10.1016/j.jhazmat.2020.123919

  • 209

    RigolettoM.CalzaP.GaggeroE.MalandrinoM.FabbriD. (2020). Bioremediation methods for the recovery of lead-contaminated soils: a review. Appl. Sci. Switz.10 (10), 3528. 10.3390/app10103528

  • 210

    RisehR. S.VazvaniM. G.HajabdollahiN.ThakurV. K. (2022). Bioremediation of heavy metals by rhizobacteria. Appl. Biochem. Biotechnol.195, 46894711. 10.1007/s12010-022-04177-z

  • 211

    RiyazuddinR.NishaN.EjazB.KhanM. I. R.KumarM.RamtekeP. W.et al (2022). A comprehensive review on the heavy metal toxicity and sequestration in plants. Biomolecules12 (1), 43. 10.3390/biom12010043

  • 212

    RizviA.KhanM. S. (2018). Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicol. Environ. Saf.157, 920. 10.1016/j.ecoenv.2018.03.063

  • 213

    RizviA.Saghir KhanM. (2019). Putative role of bacterial biosorbent in metal sequestration revealed by SEM–EDX and FTIR. Indian J. Microbiol.59 (2), 246249. 10.1007/s12088-019-00780-7

  • 214

    RizviA.ZaidiA.AmeenF.AhmedB.AlkahtaniM. D. F.KhanM. S. (2020). Heavy metal induced stress on wheat: phytotoxicity and microbiological management. RSC Adv.10 (63), 3837938403. 10.1039/d0ra05610c

  • 215

    RoyChowdhuryA.DattaR.SarkarD. (2018). “Heavy metal pollution and remediation,” in Green chemistry: an inclusive approach, 359373.

  • 216

    RussoF.CeciA.PinzariF.SicilianoA.GuidaM.MalusàE.et al (2019). Bioremediation of dichlorodiphenyltrichloroethane (DDT)- contaminated agricultural soils: potential of two autochthonous saprotrophic fungal strains. Appl. Environ. Microbiol.85 (21), e01720. 10.1128/AEM.01720-19

  • 217

    SabourianP.YazdaniG.AshrafS. S.FrounchiM.MashayekhanS.KianiS.et al (2020). Effect of physico-chemical properties of nanoparticles on their intracellular uptake. Int. J. Mol. Sci.21 (21), 80198020. 10.3390/ijms21218019

  • 218

    SahaL.TiwariJ.BauddhK.MaY. (2021). Recent developments in microbe–plant-based bioremediation for tackling heavy metal-polluted soils. Front. Microbiol.12, 731723. 10.3389/fmicb.2021.731723

  • 219

    SaibuS.AdebusoyeS. A.OyetiboG. O. (2023). Soil microbiome response to 2-chlorodibenzo-p-dioxin during bioremediation of contaminated tropical soil in a microcosm-based study. J. Hazard Mater451, 131105. 10.1016/j.jhazmat.2023.131105

  • 220

    SakshiHaritashA. K. (2020). A comprehensive review of metabolic and genomic aspects of PAH-degradation. Archives Microbiol.202 (8), 20332058. 10.1007/s00203-020-01929-5

  • 221

    SaleemS.RizviA.KhanM. J. I. J. o. E. S.Technology (2022). Microbiome-mediated nano-bioremediation of heavy metals: a prospective approach of soil metal detoxification, 124.

  • 222

    SallM. L.DiawA. K. D.Gningue-SallD.Efremova AaronS.AaronJ. J. (2020). Toxic heavy metals: impact on the environment and human health, and treatment with conducting organic polymers, a review. Environ. Sci. Pollut. Res.27 (24), 2992729942. 10.1007/s11356-020-09354-3

  • 223

    Sanchez-HernandezJ. C.NarvaezC.CaresX. A.SabatP.NaiduR. (2023). Predicting the bioremediation potential of earthworms of different ecotypes through a multi-biomarker approach. Sci. Total Environ.862, 160547. 10.1016/j.scitotenv.2022.160547

  • 224

    SapreS.Gontia-MishraI.TiwariS. (2021). Plant growth-promoting rhizobacteria ameliorates salinity stress in pea (pisum sativum). J. Plant Growth Regul.189, 647656. 10.1007/s00344-021-10329-y

  • 225

    SatyaA. D. M.CheahW. Y.YazdiS. K.ChengY. S.KhooK. S.VoD. N.et al (2023). Progress on microalgae cultivation in wastewater for bioremediation and circular bioeconomy. Environ. Res.218, 114948. 10.1016/j.envres.2022.114948

  • 226

    SayadiM. H.SalmaniN.HeidariA.RezaeiM. R. (2018). Bio-synthesis of palladium nanoparticle using Spirulina platensis alga extract and its application as adsorbent. Surfaces Interfaces10, 136143. 10.1016/j.surfin.2018.01.002

  • 227

    SchirawskiJ.HagensW.FitzgeraldG. F.Van SinderenD. J. A.microbiologye. (2002). Molecular characterization of cadmium resistance in Streptococcus thermophilus strain 4134: an example of lateral gene transfer. Appl. Environ. Microbiol.68 (11), 55085516. 10.1128/aem.68.11.5508-5516.2002

  • 228

    SenguptaD.DattaS.BiswasD.BanerjeeS.DasS. (2021). Prospective bioremediation of toxic heavy metals in water by surfactant exopolysaccharide of Ochrobactrum pseudintermedium using cost-effective substrate. Int. Microbiol.24 (3), 441453. 10.1007/s10123-021-00182-0

  • 229

    SeshadriS.SaranyaK.KowshikM. (2011). Green synthesis of lead sulfide nanoparticles by the lead resistant marine yeast, Rhodosporidium diobovatum. Biotechnol. Prog.27 (5), 14641469. 10.1002/btpr.651

  • 230

    SevakP.PushkarB.MazumdarS. (2023). Mechanistic evaluation of chromium bioremediation in Acinetobacter junii strain b2w: a proteomic approach. J. Environ. Manage328, 116978. 10.1016/j.jenvman.2022.116978

  • 231

    ShabaanM.AsgharH. N.AkhtarM. J.AliQ.EjazM. (2021). Role of plant growth promoting rhizobacteria in the alleviation of lead toxicity to Pisum sativum L. Int. J. Phytoremediation23 (8), 837845. 10.1080/15226514.2020.1859988

  • 232

    ShabbirZ.SardarA.ShabbirA.AbbasG.ShamshadS.KhalidS.et al (2020). Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment. Chemosphere259, 127436. 10.1016/j.chemosphere.2020.127436

  • 233

    SharmaP.KumarS. (2021). Bioremediation of heavy metals from industrial effluents by endophytes and their metabolic activity: recent advances. Bioresour. Technol.339, 125589. 10.1016/j.biortech.2021.125589

  • 234

    SharmaP.PandeyA. K.KimS. H.SinghS. P.ChaturvediP.VarjaniS. (2021). Critical review on microbial community during in-situ bioremediation of heavy metals from industrial wastewater. Environ. Technol. Innovation24, 101826. 10.1016/j.eti.2021.101826

  • 235

    SherS.RehmanA. (2019). Use of heavy metals resistant bacteria-a strategy for arsenic bioremediation. Appl. Microbiol. Biotechnol.103 (15), 60076021. 10.1007/s00253-019-09933-6

  • 236

    ShiT.FangL.QinH.ChenY.WuX.HuaR. (2019). Rapid biodegradation of the organophosphorus insecticide chlorpyrifos by Cupriavidus nantongensis X1(T). Int. J. Environ. Res. Public Health16 (23), 4593. 10.3390/ijerph16234593

  • 237

    SiguaG. C.NovakJ. M.WattsD. W.IppolitoJ. A.DuceyT. F.JohnsonM. G.et al (2019). Phytostabilization of Zn and Cd in mine soil using corn in combination with biochars and manure-based compost. Environ. - MDPI6 (6), 69. 10.3390/environments6060069

  • 238

    SilviantiF.ManiarD.BoetjeL.LoosK. (2020). Green pathways for the enzymatic synthesis of furan-based polyesters and polyamides. (United States: ACS Symposium Series), 329.

  • 239

    SinghE.OsmaniR. A. M.BanerjeeR. (2020). “Nanobioremediation: an emerging approach for a cleaner environment,” in Microbial bioremediation & biodegradation, 309363.

  • 240

    SobolevD.BegoniaM. F. T. (2008). Effects of heavy metal contamination upon soil microbes: lead-induced changes in general and denitrifying microbial communities as evidenced by molecular markers. Int. J. Environ. Res. Public Health5 (5), 450456. 10.3390/ijerph5050450

  • 241

    SoleimaniM.HajabbasiM. A.AfyuniM.MirlohiA.BorggaardO. K.HolmP. E. (2010). Effect of endophytic fungi on cadmium tolerance and bioaccumulation by Festuca arundinacea and Festuca pratensis. Int. J. Phytoremediation12 (6), 535549. 10.1080/15226510903353187

  • 242

    SongB.ZengG.GongJ.LiangJ.XuP.LiuZ.et al (2017). Evaluation methods for assessing effectiveness of in situ remediation of soil and sediment contaminated with organic pollutants and heavy metals. Environ. Int.105, 4355. 10.1016/j.envint.2017.05.001

  • 243

    SongX.ZhangJ.PengC.LiD. (2021). Replacing nitrogen fertilizer with nitrogen-fixing cyanobacteria reduced nitrogen leaching in red soil paddy fields. Agric. Ecosyst. Environ.312, 107320. 10.1016/j.agee.2021.107320

  • 244

    SreedeviP. R.SureshK.JiangG. (2022). Bacterial bioremediation of heavy metals in wastewater: a review of processes and applications. J. Water Process Eng.48, 102884. 10.1016/j.jwpe.2022.102884

  • 245

    SubramaniyamV.SubashchandraboseS. R.ThavamaniP.MegharajM.ChenZ.NaiduR. (2015). Chlorococcum sp. MM11—a novel phyco-nanofactory for the synthesis of iron nanoparticles. J. Appl. Phycol.27 (5), 18611869. 10.1007/s10811-014-0492-2

  • 246

    SukulP.KumarJ.RaniA.AbdillahiA. M.RakeshR. B.KumarM. H. (2021). Functioning of plant growth promoting rhizobacteria (PGPR) and their mode of actions: an overview from chemistry point of view. Plant Arch.21, 628634. 10.51470/PLANTARCHIVES.2021.v21.S1.096

  • 247

    SukweenadhiJ.KimY. J.ChoiE. S.KohS. C.LeeS. W.KimY. J.et al (2015). Paenibacillus yonginensis DCY84T induces changes in Arabidopsis thaliana gene expression against aluminum, drought, and salt stress. Microbiol. Res.172, 715. 10.1016/j.micres.2015.01.007

  • 248

    SunG. L.ReynoldsE. E.BelcherA. M. (2020). Using yeast to sustainably remediate and extract heavy metals from waste waters. Nat. Sustain.3 (4), 303311. 10.1038/s41893-020-0478-9

  • 249

    SunY.GaoK.ZhangY.ZouH. (2017). Remediation of persistent organic pollutant-contaminated soil using biosurfactant-enhanced electrokinetics coupled with a zero-valent iron/activated carbon permeable reactive barrier. Environ. Sci. Pollut. Res. Int.24 (36), 2814228151. 10.1007/s11356-017-0371-x

  • 250

    SunandaS.MisraM.Ghosh SachanS. (2022). Nanobioremediation of heavy metals: perspectives and challenges. J. Basic Microbiol.62 (3-4), 428443. 10.1002/jobm.202100384

  • 251

    SureshG.BalasubramanianB.RavichandranN.RameshB.KamyabH.VelmuruganP.et al (2021). Bioremediation of hexavalent chromium-contaminated wastewater by Bacillus thuringiensis and Staphylococcus capitis isolated from tannery sediment. Biomass Convers. Biorefinery11 (2), 383391. 10.1007/s13399-020-01259-y

  • 252

    SyedK.ShaleK.PagadalaN. S.TuszynskiJ. (2014). Systematic identification and evolutionary analysis of catalytically versatile cytochrome P450 monooxygenase families enriched in model basidiomycete fungi. PLoS ONE9 (1), e86683. 10.1371/journal.pone.0086683

  • 253

    SyedZ.SoganiM.RajvanshiJ.SonuK. (2022). Microbial biofilms for environmental bioremediation of heavy metals: a review. Appl. Biochem. Biotechnol.195, 56935711. 10.1007/s12010-022-04276-x

  • 254

    SytarO.GhoshS.MalinskaH.ZivcakM.BresticM. (2021). Physiological and molecular mechanisms of metal accumulation in hyperaccumulator plants. Physiol. Plant.173 (1), 148166. 10.1111/ppl.13285

  • 255

    TakáčováA.SmolinskáM.RybaJ.MackuľakT.JokrllováJ.HronecP.et al (2014). Biodegradation of benzo[a]Pyrene through the use of algae. Central Eur. J. Chem.12 (11), 11331143. 10.2478/s11532-014-0567-6

  • 256

    TalukdarD.JasrotiaT.SharmaR.JaglanS.KumarR.VatsR.et al (2020). Evaluation of novel indigenous fungal consortium for enhanced bioremediation of heavy metals from contaminated sites. Environ. Technol. Innovation20, 101050. 10.1016/j.eti.2020.101050

  • 257

    TambatV. S.PatelA. K.ChenC. W.RajT.ChangJ. S.SinghaniaR. R.et al (2023). A sustainable vanadium bioremediation strategy from aqueous media by two potential green microalgae. Environ. Pollut.323, 121247. 10.1016/j.envpol.2023.121247

  • 258

    TanS. Y.PraveenaS. M.AbidinE. Z.CheemaM. S. (2016). A review of heavy metals in indoor dust and its human health-risk implications. Rev. Environ. Health31 (4), 447456. 10.1515/reveh-2016-0026

  • 259

    TauqeerH. M.AliS.RizwanM.AliQ.SaeedR.IftikharU.et al (2016). Phytoremediation of heavy metals by Alternanthera bettzickiana: growth and physiological response. Ecotoxicol. Environ. Saf.126, 138146. 10.1016/j.ecoenv.2015.12.031

  • 260

    TessaroA. P. G.de AraujoL. G.SilvaT. T.CoelhoE.CorreaB.RolindoN. C.et al (2023). Prospects for fungal bioremediation of unburied waste packages from the Goiania radiological accident. Environ. Sci. Pollut. Res. Int.30, 4104541059. 10.1007/s11356-023-25247-7

  • 261

    ThakurK.KuthialaT.SinghG.AryaS. K.IwaiC. B.RavindranB.et al (2023). An alternative approach towards nitrification and bioremediation of wastewater from aquaponics using biofilm-based bioreactors: a review. Chemosphere316, 137849. 10.1016/j.chemosphere.2023.137849

  • 262

    ThakurM.PathaniaD. (2019). “Environmental fate of organic pollutants and effect on human health,” in Abatement of environmental pollutants: trends and strategies, 245262.

  • 263

    ThokchomE.ThakuriaD.KalitaM. C.SharmaC. K.TalukdarN. C. (2017). Root colonization by host-specific rhizobacteria alters indigenous root endophyte and rhizosphere soil bacterial communities and promotes the growth of Mandarin orange. Eur. J. Soil Biol.79, 4856. 10.1016/j.ejsobi.2017.02.003

  • 264

    TibiF.CharfiA.ChoJ.KimJ. (2020). Fabrication of polymeric membranes for membrane distillation process and application for wastewater treatment: critical review. Process Safety and Environmental Protection141, 190201.

  • 265

    TitchouF. E.ZazouH.AfangaH.El GaaydaJ.AkbourR. A.HamdaniM. (2021). Removal of Persistent Organic Pollutants (POPs) from water and wastewater by adsorption and electrocoagulation process. Groundw. Sustain. Dev.13, 100575. 10.1016/j.gsd.2021.100575

  • 266

    TorabiaN.KardelF. (2019). Biosorption of nickel by halobacillus sp. Kn57 isolated from the miankaleh wetland, Iran. Int. J. Aquatic Biol.7 (5), 280290. 10.22034/ijab.v7i5.704

  • 267

    TouliabahH. E. S.El-SheekhM. M.IsmailM. M.El-KassasH. (2022). A review of microalgae-and cyanobacteria-based biodegradation of organic pollutants. Molecules27 (3), 1141. 10.3390/molecules27031141

  • 268

    TufailM. A.IltafJ.ZaheerT.TariqL.AmirM. B.FatimaR.et al (2022). Recent advances in bioremediation of heavy metals and persistent organic pollutants: a review. Sci. Total Environ.850, 157961. 10.1016/j.scitotenv.2022.157961

  • 269

    TyagiB.KumarN. (2020). “Bioremediation: principles and applications in environmental management,” in Bioremediation for environmental sustainability: toxicity, mechanisms of contaminants degradation, detoxification and challenges, 328.

  • 270

    Ubaid ur RahmanH.AsgharW.NazirW.SandhuM. A.AhmedA.KhalidN. (2021). A comprehensive review on chlorpyrifos toxicity with special reference to endocrine disruption: evidence of mechanisms, exposures and mitigation strategies. Sci. Total Environ.755, 142649. 10.1016/j.scitotenv.2020.142649

  • 271

    UllahA.MaY.LiJ.TahirN.HussainB. (2020). Effective amendments on cadmium, arsenic, chromium and lead contaminated paddy soil for rice safety. Agronomy10 (3), 359. 10.3390/agronomy10030359

  • 272

    UllahN.RehmanM. U.AhmadB.AliI.YounasM.AslamM. S.et al (2022). Assessment of heavy metals accumulation in agricultural soil, vegetables and associated health risks. PLoS ONE17 (6 June), e0267719. 10.1371/journal.pone.0267719

  • 273

    UllahS.BanoA. (2015). Isolation of plant-growth-promoting rhizobacteria from rhizospheric soil of halophytes and their impact on maize (Zea mays L.) under induced soil salinity. Can. J. Microbiol.61 (4), 307313. 10.1139/cjm-2014-0668

  • 274

    UsmanM.FarooqM.WakeelA.NawazA.CheemaS. A.RehmanH. U.et al (2020). Nanotechnology in agriculture: current status, challenges and future opportunities. Sci. Total Environ.721, 137778. 10.1016/j.scitotenv.2020.137778

  • 275

    Valentim dos SantosJ.Varón-LópezM.Fonsêca Sousa SoaresC. R.Lopes LealP.SiqueiraJ. O.de Souza MoreiraF. M. (2016). Biological attributes of rehabilitated soils contaminated with heavy metals. Environ. Sci. Pollut. Res.23 (7), 67356748. 10.1007/s11356-015-5904-6

  • 276

    VallsM.AtrianS.De LorenzoV.FernándezL. A. (2000). Engineering a mouse metallothionein on the cell surface of Ralstonia eutropha CH34 for immobilization of heavy metals in soil. Nat. Biotechnol.18 (6), 661665. 10.1038/76516

  • 277

    VanisreeC. R.SankhlaM. S.SinghP.JadhavE. B.VermaR. K.AwasthiK. K.et al (2022). Heavy metal contamination of food crops: transportation via food chain. Hum. Consum. Toxic. Manag. Strateg.

  • 278

    VermaN.JujjavarapuS. E.MahapatraC.MutraJ. K. R. (2023). Contemporary updates on bioremediation applications of graphene and its composites. Environ. Sci. Pollut. Res. Int.30, 4885448867. 10.1007/s11356-023-26225-9

  • 279

    VermaN.SharmaR. (2017). Bioremediation of toxic heavy metals: a patent review. Recent Pat. Biotechnol.11 (3), 171187. 10.2174/1872208311666170111111631

  • 280

    WanW.QinY.WuH.ZuoW.HeH.TanJ.et al (2020). Isolation and characterization of phosphorus solubilizing bacteria with multiple phosphorus sources utilizing capability and their potential for lead immobilization in soil. Front. Microbiol.11, 752. 10.3389/fmicb.2020.00752

  • 281

    WangL.HouD.ShenZ.ZhuJ.JiaX.OkY. S.et al (2020). Field trials of phytomining and phytoremediation: a critical review of influencing factors and effects of additives. Crit. Rev. Environ. Sci. Technol.50 (24), 27242774. 10.1080/10643389.2019.1705724

  • 282

    WangP.HuX.HeQ.WaigiM. G.WangJ.LingW. (2018). Using calcination remediation to stabilize heavy metals and simultaneously remove polycyclic aromatic hydrocarbons in soil. Int. J. Environ. Res. Public Health15 (8), 1731. 10.3390/ijerph15081731

  • 283

    WangQ.ZhangW. J.HeL. Y.ShengX. F. (2018). Increased biomass and quality and reduced heavy metal accumulation of edible tissues of vegetables in the presence of Cd-tolerant and immobilizing Bacillus megaterium H3. Ecotoxicol. Environ. Saf.148, 269274. 10.1016/j.ecoenv.2017.10.036

  • 284

    WangX.ZhangD.PanX.LeeD. J.Al-MisnedF. A.MortuzaM. G.et al (2017). Aerobic and anaerobic biosynthesis of nano-selenium for remediation of mercury contaminated soil. Chemosphere170, 266273. 10.1016/j.chemosphere.2016.12.020

  • 285

    WangZ.WangH.NieQ.DingY.LeiZ.ZhangZ.et al (2023a). Pb(II) bioremediation using fresh algal-bacterial aerobic granular sludge and its underlying mechanisms highlighting the role of extracellular polymeric substances. J. Hazard Mater444 (Pt B), 130452. 10.1016/j.jhazmat.2022.130452

  • 286

    WangZ.ZhangJ.DaiY.ZhangL.GuoJ.XuS.et al (2023b). Mediating effect of endocrine hormones on association between per- and polyfluoroalkyl substances exposure and birth size: findings from sheyang mini birth cohort study. Environ. Res.115658, 115658. 10.1016/j.envres.2023.115658

  • 287

    WeiZ.Van LeQ.PengW.YangY.YangH.GuH.et al (2021). A review on phytoremediation of contaminants in air, water and soil. J. Hazard. Mater.403, 123658. 10.1016/j.jhazmat.2020.123658

  • 288

    WickramasingheW.GirijaD.GopalK. S.KesevanS. (2021). Multi-phasic nitrogen fixing plant growth promoting rhizobacteria as biofertilizer for rice cultivation. Res. J. Agric. Sci.12, 399404.

  • 289

    WuX.HuangP.DongC.DengX. (2021). Nickel bioaccumulation by a marine bacterium Brevibacterium sp. (X6) isolated from Shenzhen Bay, China. Mar. Pollut. Bull.170, 112656. 10.1016/j.marpolbul.2021.112656

  • 290

    WuZ.YuF.SunX.WuS.LiX.LiuT.et al (2018). Long term effects of Lespedeza bicolor revegetation on soil bacterial communities in Dexing copper mine tailings in Jiangxi Province, China. Appl. Soil Ecol.125, 192201. 10.1016/j.apsoil.2018.01.011

  • 291

    WyszkowskaJ.BorowikA.KucharskiM.KucharskiJ. (2013). Effect of cadmium, copper and zinc on plants, soil microorganisms and soil enzymes. J. Elem.18 (4), 769796. 10.5601/jelem.2013.18.4.455

  • 292

    XiaX.LinS.ZhaoJ.ZhangW.LinK.LuQ.et al (2018). Toxic responses of microorganisms to nickel exposure in farmland soil in the presence of earthworm (Eisenia fetida). Chemosphere192, 4350. 10.1016/j.chemosphere.2017.10.146

  • 293

    XiangY.XingZ.LiuJ.QinW.HuangX. (2020). Recent advances in the biodegradation of polychlorinated biphenyls. World J. Microbiol. Biotechnol.36 (10), 145. 10.1007/s11274-020-02922-2

  • 294

    XieY.FanJ.ZhuW.AmomboE.LouY.ChenL.et al (2016). Effect of heavy metals pollution on soil microbial diversity and bermudagrass genetic variation. Front. Plant Sci.7 (MAY2016), 755. 10.3389/fpls.2016.00755

  • 295

    XuY.WangS.LiL.SahuS. K.PetersenM.LiuX.et al (2019). Molecular evidence for origin, diversification and ancient gene duplication of plant subtilases (SBTs). Sci. Rep.9 (1), 12485. 10.1038/s41598-019-48664-6

  • 296

    YadavK. K.SinghJ. K.GuptaN.KumarV. (2017). A review of nanobioremediation technologies for environmental cleanup: a novel biological approach. J. Mater. Environ. Sci.8 (2), 740757.

  • 297

    YanF. F.WuC.ChengY. Y.HeY. R.LiW. W.YuH. Q. (2013). Carbon nanotubes promote Cr(VI) reduction by alginate-immobilized Shewanella oneidensis MR-1. Biochem. Eng. J.77, 183189. 10.1016/j.bej.2013.06.009

  • 298

    YangJ.CaoJ.XingG.YuanH. (2015). Lipid production combined with biosorption and bioaccumulation of cadmium, copper, manganese and zinc by oleaginous microalgae Chlorella minutissima UTEX2341. Bioresour. Technol.175, 537544. 10.1016/j.biortech.2014.10.124

  • 299

    YangQ.GuoY.XiangY.ChenL.LiuG.LiuY.et al (2023). Toward efficient bioremediation of methylmercury in sediment using merB overexpressed Escherichia coli. Water Res.229, 119502. 10.1016/j.watres.2022.119502

  • 300

    YangX.LiuL.TanW.LiuC.DangZ.QiuG. (2020). Remediation of heavy metal contaminated soils by organic acid extraction and electrochemical adsorption. Environ. Pollut.264, 114745. 10.1016/j.envpol.2020.114745

  • 301

    YangY.ZhouX.TieB.PengL.LiH.WangK.et al (2017). Comparison of three types of oil crop rotation systems for effective use and remediation of heavy metal contaminated agricultural soil. Chemosphere188, 148156. 10.1016/j.chemosphere.2017.08.140

  • 302

    YangY.-C.HuangW.-S.HuS.-M.HuangC.-W.ChiuC.-H.ChenH.-Y. J. P. (2020). Synergistic and regulatable bioremediation capsules fabrication based on vapor-phased encapsulation of bacillus bacteria and its regulator by poly-p-Xylylene. Polym. (Basel).13 (1), 41. 10.3390/polym13010041

  • 303

    YanitchA.KadriH.Frenette-DussaultC.JolyS.PitreF. E.LabrecqueM. (2020). A four-year phytoremediation trial to decontaminate soil polluted by wood preservatives: phytoextraction of arsenic, chromium, copper, dioxins and furans. Int. J. Phytoremediation22, 15051514. 10.1080/15226514.2020.1785387

  • 304

    Yetunde MutiatF.-B.GbolahanB.OluO. J. B. J. (2018). A comparative study of the wild and mutated heavy metal resistant Klebsiella variicola generated for cadmium bioremediation. Bioremediat. J.22 (1-2), 2842. 10.1080/10889868.2018.1445695

  • 305

    YuY.ShiK.LiX.LuoX.WangM.LiL.et al (2022). Reducing cadmium in rice using metallothionein surface-engineered bacteria WH16-1-MT. Environ. Res.203, 111801. 10.1016/j.envres.2021.111801

  • 306

    Zafar-ul-HyeM.Tahzeeb-ul-HassanM.AbidM.FahadS.BrtnickyM.DokulilovaT.et al (2020). Potential role of compost mixed biochar with rhizobacteria in mitigating lead toxicity in spinach. Sci. Rep.10 (1), 12159. 10.1038/s41598-020-69183-9

  • 307

    ZanganehF.HeidariA.SepehrA.RohaniA. (2022). Bioaugmentation and bioaugmentation–assisted phytoremediation of heavy metal contaminated soil by a synergistic effect of cyanobacteria inoculation, biochar, and purslane (Portulaca oleracea L.). Environ. Sci. Pollut. Res.29 (4), 60406059. 10.1007/s11356-021-16061-0

  • 308

    ZaynabM.Al-YahyaiR.AmeenA.SharifY.AliL.FatimaM.et al (2022). Health and environmental effects of heavy metals. J. King Saud Univ. - Sci.34 (1), 101653. 10.1016/j.jksus.2021.101653

  • 309

    ZhaiX.LiZ.HuangB.LuoN.HuangM.ZhangQ.et al (2018). Remediation of multiple heavy metal-contaminated soil through the combination of soil washing and in situ immobilization. Sci. Total Environ.635, 9299. 10.1016/j.scitotenv.2018.04.119

  • 310

    ZhanF.LiB.JiangM.LiT.HeY.LiY.et al (2019). Effects of arbuscular mycorrhizal fungi on the growth and heavy metal accumulation of bermudagrass [Cynodon dactylon (L.) Pers.] grown in a lead–zinc mine wasteland. Int. J. Phytoremediation21 (9), 849856. 10.1080/15226514.2019.1577353

  • 311

    ZhangJ.WangX.ZhangL. X.ZhaoF. J. (2021). Reducing cadmium bioavailability and accumulation in vegetable by an alkalizing bacterial strain. Sci. Total Environ.758, 143596. 10.1016/j.scitotenv.2020.143596

  • 312

    ZhangL.LiuW.LiuS.ZhangP.YeC.LiangH. (2020). Revegetation of a barren rare earth mine using native plant species in reciprocal plantation: effect of phytoremediation on soil microbiological communities. Environ. Sci. Pollut. Res.27 (2), 21072119. 10.1007/s11356-019-06645-2

  • 313

    ZhangW.ZhangH.XuR.QinH.LiuH.ZhaoK. (2023). Heavy metal bioremediation using microbially induced carbonate precipitation: key factors and enhancement strategies. Front. Microbiol.14, 1116970. 10.3389/fmicb.2023.1116970

  • 314

    ZhaoX.ZengX.QinY.LiX.ZhuT.TangX. (2018). An experimental and theoretical study of the adsorption removal of toluene and chlorobenzene on coconut shell derived carbon. Chemosphere206, 285292. 10.1016/j.chemosphere.2018.04.126

  • 315

    ZhouH.GaoX.WangS.ZhangY.CoulonF.CaiC. (2023a). Enhanced bioremediation of aged polycyclic aromatic hydrocarbons in soil using immobilized microbial consortia combined with strengthening remediation strategies. Int. J. Environ. Res. Public Health20 (3), 1766. 10.3390/ijerph20031766

  • 316

    ZhouX.ZhangS.WangR.AnZ.SunF.ShenC.et al (2023b). A novel strategy for enhancing bioremediation of polychlorinated biphenyl-contaminated soil with resuscitation promoting factor and resuscitated strain. J. Hazard Mater447, 130781. 10.1016/j.jhazmat.2023.130781

  • 317

    ZhuJ.ZhaoY. A. N.RuanH. (2019). Comparative study on the biodegradation of chlorpyrifos-methyl by bacillus megaterium CM-Z19 and pseudomonas syringae CM-Z6. An. Acad. Bras. Ciencias91 (3), e20180694. 10.1590/0001-3765201920180694

  • 318

    ZhuM.YinH.YuanY.QiX.LiuH.WeiX.et al (2022). Promotion of the biodegradation of phenanthrene adsorbed on microplastics by the functional bacterial consortium QY1 in the presence of humic acid: bioavailability and toxicity evaluation. Environ. Pollut.307, 119591. 10.1016/j.envpol.2022.119591

  • 319

    ZhuN.ZhangB.YuQ. (2020). Genetic engineering-facilitated coassembly of synthetic bacterial cells and magnetic nanoparticles for efficient heavy metal removal. ACS Appl. Mater. Interfaces12 (20), 2294822957. 10.1021/acsami.0c04512

  • 320

    ZhuoR.FanF. (2021). A comprehensive insight into the application of white rot fungi and their lignocellulolytic enzymes in the removal of organic pollutants. Sci. Total Environ.778, 146132. 10.1016/j.scitotenv.2021.146132

  • 321

    ZwolakA.SarzyńskaM.SzpyrkaE.StawarczykK. (2019). Sources of soil pollution by heavy metals and their accumulation in vegetables: a review. Water, Air, Soil Pollut.230 (7), 164. 10.1007/s11270-019-4221-y

Summary

Keywords

heavy metals, nano-bioremediation, PGPR, phytoremediation, pollution

Citation

Karnwal A, Martolia S, Dohroo A, Al-Tawaha ARMS and Malik T (2024) Exploring bioremediation strategies for heavy metals and POPs pollution: the role of microbes, plants, and nanotechnology. Front. Environ. Sci. 12:1397850. doi: 10.3389/fenvs.2024.1397850

Received

08 March 2024

Accepted

17 July 2024

Published

31 July 2024

Volume

12 - 2024

Edited by

Khandaker Rayhan Mahbub, Primary Industries and Resources South Australia, Australia

Reviewed by

Neha Pandey, Pandit Ravishankar Shukla University, India

Padmanabh Dwivedi, Banaras Hindu University, India

Updates

Copyright

*Correspondence: Arun Karnwal, ; Tabarak Malik,

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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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