Editorial: "Xenobiotic and Emerging Contaminants in Ecosystems: Innovative Geomicrobial Strategies for Prevention, Efficient Clean-up and Biosafety"

Balaram Mohapatra^1*Avishek Dutta^1*Prashant S Phale²Upendra Kumar¹

• ¹Gujarat Biotechnology University, Gandhinagar, India
• ²iit, bombay, India

Anthropogenic emissions and industrial discharge of toxic xenobiotic organic compounds i.e. (un)saturated hydrocarbons, aromatics (mono/poly-aromatics) and their substituted derivatives as history contaminants, emerging-(pharmaceuticals and personal care products (PPCPs), micro/nano plastics, nanomaterials), forever -chemicals are creating dire ecological consequences (Summarized in Fig. 1) (Mohapatra and Phale, 2022). The Environmental Protection Agency (EPA) has prioritized 129 of such compounds (acenaphthene being the 1 st on the list) that are regulated under the Clean Water Act (https://www.epa.gov/sites/default/files/2015-09/documents/priority-pollutant-list-epa.pdf).The majority of them are highly hydrophobic (higher LogPow), genotoxic, mutagenic, having endocrine disrupting-(cholinergic excess, hormone analogs, transport inhibitors, etc.) and cytotoxic-activities (form adducts, induce lipid peroxidation, impair CYP450 function, depurination, permeabilization of membranes, disruption in energy transduction, etc.) (Mohapatra and Phale, 2021). A few are classified as human carcinogens, e.g. polychlorinated biphenyls (PCBs), polychlorinated dibenzofurans (PCDFs) with a higher bio-accumulative nature. These chemicals are found to be in various forms i.e., aerosols, fumes, particulates, liquids, and deposits, and can transfer through percolation, run-off, advection, infiltration, and other secondary processes (co-ordination/co-complexation/co-precipitation, etc.); thus, severely impacting the ecosystem's biogeochemical functions (Gonzalez-Gaya et al., 2019). Alternatively, these xenobiotics exerted selective pressure on natural microbiota to evolve adaptive and metabolic strategies to overcome their toxic effects, survive, and attenuate such effects at the impacted sites. However, various hurdles, e.g. environmental cues (lack of essential nutrients, inhibitory factors, redox dynamics), microbial/cellular factors (availability of electron donors/acceptors, carbon repression, species competition, regulation of enzyme induction, eco-physiology traits, etc.), and physico-chemical conditions (type, concentration, mass balance, bioavailability) render the process ineffective at the field scale (Phale et al., 2020). Though use of multi-OMICS technologies including meta-genomics (environmental DNA), transcriptomics (RNAs), proteomics (cellular/sub-scellular proteins), metabolomics (metabolites), mobilomics (mobile genetic elements), and fluxomics (metabolic flux) combined with advanced bioinformatic tools have provided new insights into underlying mechanisms of such field-scale bioremediation/containment, the extent of efficacy (because of colonization resistance) and sustainability remains to be unanswered (Sharma et al., 2022). Traditional and new-age engineering bioremediation reactions based on synthetic biology/metabolic engineering has worked well under in-vitro/discrete locations, but they have not yet been fully implemented at in-vivo/large-scale/planet-wide settings, possibly due to rate-limiting biology/enzymology steps (de Lorenzo, 2022). Hence, a multi-sectoral effort on assessing the ecotoxicology and biosafety of these compounds, with prevention of its ecosystem entry, advanced-ecofriendly-cum-deployable abatement technologies and bioprocesses (in-situ/ex-situ and engineered) is a must for effective clean-up (Kuppan et al., 2024;Visvanathan et al., 2024). Considering the urgency of the situation, a research topic was hosted on understanding the toxic and hazardous xenobiotic emerging contaminants in ecosystems and innovative geo-microbial strategies for efficient Clean-up and biosafety. A total of five manuscripts were submitted in this issue, out of which one article was rejected and four were published. This editorial article on this research topic emphasizes the effective strategies for cleaning up such xenobiotics, thus reducing potential risks of exposure to biota.According to Shah et al., microbe-mediated strategies (metabolic, genetic and enzymatic) for tackling contaminants of emerging concern (CEC: pharmaceuticals, personal care products, nanomaterials, pesticides, plasticizers, microplastics, cyano-/algal-toxins, and PFOS/PFAS) are of utmost importance for clean-up. The detection of such compounds can be attributed either to their recent introduction into the environment or an advancement in detection technologies, but with poorly understood risk profiles (Podder et al., 2021). However, microbial candidates are able to utilize them as a source of carbon/nitrogen, energy, and electrons with dynamic metabolic diversity, which could work as an eco-friendly alternative to mitigate their toxicity. For example, the bacterium, Bacillus cereus H38, was shown to possess two pathways i.e. S-N bond cleavage and N 4 -amine cleavage for sulfonamide degradation, and Pseudomonas psychrophila HA-4 for sulfomethoxazole (hydroxy and amino-benzenesulfonamide). Involvement of inducible enzymes like flavin-dependent monoxygenases, FMN reductase, and 1,4-benzoquinone reductase have been reported in a wide variety of taxa. The role of the consortium (XG) consisting of species of Achromobacter, Bacillus, Lactococcus, Ochrobactrum, and Enterococcus has also been reported for the mineralization of other antibiotics. For analgesics, Sphingomonas sp. Ibu-2 is reported to convert ibuprofen to ibuprofen-CoA by the action of a CoAligase, followed by isobutylcatechol and then meta-ring cleavage. Whereas Variovorax sp. Ibu-1 metabolizes ibuprofen via the formation of trihydroxyibuprofen, which then undergoes meta-ring cleavage to form aliphatic intermediates mediated by the ipfABDEF gene cluster. Interestingly, Sphingopyxis-mediated clearance (through formation of phenylacetic acid derivatives) of harmful algal bloom (due to eutrophication), releasing cyanotoxins (microcystins and nodularin: complex species of cyclic penta-and hexapeptides), is highlighted. In case of plasticizers (phthalate esters isomers of mid and long chain) which are reported as potent endocrine-disrupting chemicals (EDCs), metabolism by Gordonia, Rhodococcus, Pseudomonas, Cupravidus, Burkholderia, Achromobacter, Agromyces, Microbacterium, Acinetobacter, and Bacillus is reported. The initial degradation occurs through either a) de-esterification leading to the formation of mono-alkyl esters like conversion of DEHP to mono-(2ethyhexyl) phthalate (MEHP), then further to phthalic acid, or b) stepwise beta-oxidation of alkyl side chains like conversion through intermediates like diethyl phthalate (DEP), mono-methyl phthalate (MMP), or butyl methyl phthalate (BMP) and ultimately funnels to central carbon pathways. The metabolic routes and enzymes involved in degradation of most commonly used benzene-based pesticides (imidacloprid and chlorpyrifos) and herbicide (glyphosate) are also underlined displaying special mention of metal-dependant enzymes i.e. hydrolases (organophosphorus hydrolase, phosphotriesterase, methyl parathion hydrolase and organophosphorus acid anhydrolase), thus reducing the toxicity and activating the compounds for better degradation. The importance of multi-omics approaches like genomics in conjunction with transcriptomics and proteomics to identify up/downregulation of genes/proteins under target conditions are emphasized. Considering the limitations e.g. slow degradation rates, incomplete transformation, reduced survivability, etc. of using bacterial strains/cultures/consortia at the site, use of directed genetic engineering, "metabolic engineering" is proposed to enhance the metabolic diversity, degradation rates, physiological vigour, and to overcome carbon catabolite repression, thus offering potential research opportunities.Persistent oil hydrocarbons (OHs: alkane and aromatics and their substituted n-mers) discharged from spillage, refinery extraction, pipelines, and service stations mostly lead to soil, food, and groundwater contamination. In this research topic, Melzi et al. highlighted the use of phytoremediation (microbe-assisted) as an ideal solution to eliminate or decrease the concentration of OHs. The authors presented an example of phytoremediation-based bioremediation intervention for OHs (both C≤12 and C>12) spilled from the oil spillage site to the aquifer and the wetland soil having Scirpus sylvaticus (L.). Prevalence of diatoms (Ulnaria spp.) were identified as bioindicator spp. Soil microcosm indicated reduction of OHs phytotoxicity and phytodegradation (upto 82%) when treated to Zea mays and Helianthus annuus. It has been also demonstrated that involvement of functional genes encoding toluene-benzene monooxygenase (tbmD) and alkane hydroxylase (alkB) enabled the community to achieve higher biodegradation rates, thus indicating a natural bio-attenuation process and possible application for site recovery.With respect to high energy demand and dependency on carbon-neutral economy, better bioprospection of coal mine and its waste/waste coal requires major attention. Coalbed methane (CBM) has emerged as an important energy source in developing nations like India and is expected to play a significant role in the energy portfolio of the future. Basera et al. has reported enhanced methane production from lignite (lowest-rank coal) by optimization of the bioconversion to methane at 55 °C temperature and 0.15% of NaCl concentration. A scale-up study demonstrated higher methane yield (2800 mM methane per 25 g of lignite) under anaerobic conditions, where bioconversion route and intermediates were confirmed through fourier transform infrared (FTIR) and gas chromatography mass spectrometry (GC-MS). The authors highlighted that a bacterial consortiium converted lignite into volatile fatty acids, which was subsequently converted into methane by Methanosarcinales and Methanomicrobiales. Thus, it showed the prospect of developing indigenous consortia that can potentially enhance methane production from the low-rank coal in Indian coal beds under thermophilic conditions.Discharge of radioactive waste from nuclear power plants, nuclear weapon tests, and medical procedures releases dangerous radioactive iodine isotopes into the environment. Duborska et al. highlighted the importance of eliminating iodine radionuclides (36 known radioactive isotopes of iodine, like 129 I and 131 I, majorly occur as iodate) from the polluted environment. Though physicochemical methods (metal oxide chelation, bentonite clay adsorption, biomass composite) are attempted, microbial iodine speciation/transformation and removal has gain attention. The authors reviewed iodate reduction (by non-specific nitrate and chlorate reductase and iodate reductase) by metal-interacting bacterial members e.g. Shewanella spp., and Agrobacterium spp., for such action with reports on recruitment of key metabolites like glutathione. Shewanella oneidensis has been shown to reduce iodate extracellularly by employing outer membrane MtrAB as well membrane-bound dimethyl sulfoxide (DMSO) reductase with a molybdenum enzyme centre as a catalytic site. Strains of Roseobacter and Rhodothalassium been reported that oxidize iodine species by employing multi-copper oxidase system. Fungi like Aspergillus, which employ an oxidase to transform iodine was also highlighted. Volatilization to organic iodines (methylated forms) are also reported by Proteobacteria, Cytophaga-Flexibacter-Bacteroides and some cyanobacteria and algal spp., but the molecular details are yet to be confirmed. With higher uptake rate in microbes e.g. Ralstonia, Cupriavidus, Bacillus, Streptomyces, etc., these organisms bioaccumulate iodine into various biomass fractions, which could be explored for industrial extraction of iodine from saline and brine systems. Additionally, use of biomass-derived composite like cellulose nanocomposite, organic frameworks with metals (Zn), for sustainable iodine recovery and remediation efforts was highlighted by Duborska et al. This observation is in line with the use of biotransforming/redox-active microbes combined with plants (phytoremediation) for successful bioremediation of iodine, cesium and uranium from contaminated sites (Thakur and Kumar, 2024).Finally, we believe that the research topic on "Xenobiotic and Emerging Contaminants in Ecosystems" will provide key insights into recent advances in the use of microbial inoculants, bioprocesses, and climate-smart biotechnologies to remediate contaminated sites while preserving ecosystem health. It will also help the researchers and policymakers to rationalize effective and innovative clean-up processes, thus reducing potential risks of exposure to these contaminants.