Abstract
Biogas production via anaerobic digestion is an established and robust technology that produces energy and recycles nutrients. Several biotechnological attempts have been applied to this process to increase biogas production, including adding nanoparticles, but several discrepancies have been reported. To elucidate the contradictory results, we performed a literature review followed by a meta-analysis to evaluate the effect of adding natural nanoparticles to biogas sludge. Our results showed that adding nanoparticles can increase biogas production by up to two orders of magnitude. Considering that, we attribute these results to variability in the nanoparticles applied, leading to less reliable, consistent, and even contradictory results. We observed that the magnetite nanoparticles are the most tested ones with the most promising positive effects. In addition, we observed that concentrations of nanoparticles higher than 100 mg/L can have adverse effects, with an overall decrease in biogas production. The findings in this study highlight the need for a proper characterization of the nanomaterials type and concentration applied to the process to understand the interactions and effects on the microbial communities and dynamics that lead to an overall increase or decrease in biogas yield.
1 Introduction
Investment in renewable energy sources is a reality nowadays (). Among the different renewable energy sources, the production of biogas from organic waste, generated in the complex microbial process of anaerobic digestion (AD), stands out due to its many advantages (; ; ). AD is an integrated biological process of the decomposition of organic matter in an oxygen-free environment that produces biogas and a digestate. Biogas is mainly composed of methane (CH4), carbon dioxide (CO2) and other minor molecules (H2, H2S, N2, H2O) (; ). Although it is a promising strategy, biogas production from AD still faces challenges in its process stability and efficiency (; ). This process also deals with different groups of microorganisms that play crucial roles in AD () and the syntrophic relationship between these microorganisms, which have different growth requirements (; ), is mandatory to achieve maximum biogas production (). Thus, many strategies have been developed to improve microbial metabolic activities and biogas production in AD, such as co-digestion, pre-treatments and upgrades approaches (; ; ; ; ).
The strategy of nanoparticles (NPs) addition to the AD process has shown results in improving the stability of the microbial community and the electric exchange between organic reductive bacteria and methanogenic archaea by enhancing direct interspecies electron transfer (DIET) efficiency (; ). Conductive NPs such as magnetite and nickel would be related to the increase in electron transfer efficiency between methane-producing microorganisms and other species that inhabit biogas reactors, a process also known as “electrical syntrophy” (; ). It has also been suggested that the benefit of NPs addition may be related microbial growth requirements for trace elements, such as Fe, Ni, and Cu, for the enzymatic activity of the different microorganisms involved in AD.
NPs with different chemical compositions were studied for such purpose, like composed of silver (), zero valent iron (), cobalt (), nickel (; ), carbon () and magnetite (Fe3O4) (; ; ; Yu et al., 2022), among others (). In 2019, Jin and others were successful in increasing 3–10 times the production of biogas by using chemically synthesized magnetite NPs. The increased yield was attributed to the conductive property of magnetite to increase the efficiency of DIET ().
The benefit of the addition of NPs can also be a consequence of other NPs interactions such as the reduction of short-chain fatty acids accumulation, which in high amounts inhibits the AD process, organic matter overload, and the mitigation of H2S and ammonia, which ends up directly increasing CH4 production (; ; ; ; Ziganshina et al., 2022). Thus, the NPs could be potentially used to accelerate microbial activities in AD and optimize CH4 production. However, the outcome reported for NPs effect on biogas production is not consistent. observed an increase in biogas and CH4 production after adding iron oxide NPs that was lower than those previously observed by . In their discussion, suggested that this difference is due to different parameters in the methods between the studies, despite using NPs of similar composition. These differences include different specific composition and concentrations of NPs (Farghali used Fe2O3 at a concentration of 100 mg/L while Abdelsalam used Fe3O4 at 20 mg/L) and the substrates (Farghali tested cattle manure as substrate, while Abdelsalam used raw manure) (; ). This type of discrepancy in results emphasizes the importance of studies that allow comparison and systematizing the parameters and respective impacts of adding NPs to increase biogas production by AD.
Performing a systematic analysis is a suitable technique to integrate, in a reliable way, results from different studies to summarize its findings in more clear and robust conclusions (). In addition, conducting a meta-analysis contributes to resolving conflicting results from the literature and finding new patterns that bench experiments cannot achieve. Here, we performed a systematic review followed by a meta-analysis according to PRISMA 2020 statement (). Data collected was submitted to a series of statistical analysis to clarify NPs addition in the AD process and its implications for methane production improvement.
2 Materials and methods
2.1 Keywords, screening and data collecting
An advanced search code with the keywords “anaerobic digestion”, “biogas”, “methane” and “nanoparticles” and synonyms combined with Boolean operators (AND, OR and NOT) and wildcards (*, $) was entered with filters for English language and type of article file using the Web of Science (https://www.webofknowledge.com) database. Filters for English language, with document type for articles and time from 1997 to 2022 were used as well. Then, a preliminary screening was carried out with the following eligibility criteria in which studies should: 1) deal with a process of methane production by AD that provides methane yield data of the control and NPs treatments; 2) intentionally add and analyze NPs impact in methane production in AD; 3) provide information on the characteristics of NPs (at least composition, size and concentration added); 4) present experimental data and analysis (excluding modeling, simulations, bibliographic and systematic reviews).
After this screening step, selected articles were analyzed and data about the AD substrates type, NPs features and methane yield in the experiments (control and treatments) was collected. Information about the studies such as year of publication, author names, operational and experimental conditions were also collected. The main data collected from the selected primary publications were converted to a CSV file (Supplementary Table S1).
2.2 Statistical analysis
Data collected was submitted to the ROUT method for identifying outliers (), followed by One-way ANOVA tests of variance, followed by Fisher’s multiple test, when significant, in GraphPad Prism software version 8.02 (GraphPad, United States of America). p-value <0.05 was considered statistically significant.
Data of different treatments in which NPs were added to the AD process were grouped according to NPs composition. Their effect in CH4 yield was compared to the control (without NPs addition) was given by calculating the natural log response ratio (ratio between the mean of the experimental group and that in the control group), expressed below (Eq. 1) (). This effect size calculation was chosen due to the high number of articles that did not clearly present a measure of dispersion and which information would have been lost if only those with this information were considered.
Eq. 1 Response ratio between CH4 production in treatment groups (XT) and control groups (XC).
Using the Past software () the Kernel Density Estimation (KDE–Kernel’s density estimator) was calculated in order to provide the coordinates used for elaboration of density graphs in order to analyze the profile of the data obtained (). The KDE method allows the observation of the density profile of data distribution against two variables. In other words, it allows observing at which points regarding the two variables the data obtained are more concentrated. Pearson’s correlation tests were also performed between the variables “size (nm)” and “concentration (mg/L)”, and the improvement in CH4 production, also expressed by Hedges’ RR.
3 Results
3.1 Screening trials
The advanced search performed on the Web of Science database resulted in 877 articles. After the initial screening, 377 articles were selected for further data collection. Finally, after analysis and data collection according to the criteria described above, 290 data from 64 articles.
Different experimental conditions were used in the selected papers; for example, the volumes of the experiments varied from 25 mL flasks to 9 L reactors. Reactor models and the selected AD temperature varied. However, most of the experiments analyzed were carried out on laboratory scale, in mesophilic batch systems. Circa 68% of the tests were performed in flasks or bottles, 27% in a reactor and 5% in automatic methane potential test systems. The NPs concentrations used were displayed in different units and only those that could be converted to mg/L were kept in the analysis, resulting in these 64 articles remaining. This unit was chosen because it allowed the conversion of the largest number of studies. A great variation was also observed in expressing information related to the size of the NPs used and their origins or production methods, and the improvement of the production of CH4—which was unified by the Natural Logarithmic Response Ratio (RR CH4) described above. The main data used in the analysis of this work are displayed in Supplementary Table S1.
3.2 Impact of NPs of different compositions
Effect sizes were calculated using Natural Log Response Ratio between the CH4 production in the treatment group (with NPs) and the control (without) of every study selected. The results were grouped according to NPs composition. Different effects of the addition of each NPs composition on CH4 production were observed (Figure 1). The effect size (expressed by the RR) demonstrates how much the treatment (NPs addition) has a positive or negative effect compared to when no NPs are added. When the 95% CI lines overcross the 0 point, it means that the NPs may cause inhibitory effects. When the middle circle (representing the mean RR CH4 of each group) undercrosses the 0 line, it represents a major probability in causing inhibitory rather than stimulatory effects in AD. Thus, certain NPs are more related to increased methane production, while others demonstrate more impacts that are negative on AD (Figure 1). The NPs with the best effects for increasing CH4 production are those composed of cobalt, zero valent iron and magnetite. Zinc oxide as well as copper oxide showed more inhibitory than beneficial effects.
FIGURE 1
Some NPs were tested in different types of substrates, such as magnetite and zero valent iron, but a wide range of other compositions was restricted to a few specific substrates. Only magnetite had its effect evaluated for all categories of substrates. For all of them this NPs composition presents, on average, better results (Figures 1A, D). As magnetite was the only tested on all studied substrates, it allowed us to make a specific comparison of those NPs on all substrates (Figure 1D). Here, we compared magnetite NPs results with those of cobalt (Figure 1B) and zero valent iron NPs (Figure 1C). Every color point represents one size effect of NPs impact in CH4 production by DA (Figure 1). On average, magnetite had a positive effect stimulating the biogas production when added to all substrates (Figure 1D). NPs composed by zero valent iron also stimulated biogas production, except when added to synthetic medium (Figure 1C). These results highlight the need for proper testing the effects of different NPs applied to different substrates. It is also relevant to evaluate each AD process in a wide point of view, comparing NPs characteristics, microbial community and biochemical changes to achieve a more complex understanding of its effects.
3.3 Impact of NPs concentration and size
The surface analysis generated by the Kernel’s density estimator (KDE–Kernel’s density estimator) indicated that the increase in the size or concentration of the NPs used in the AD process did not result in greater beneficial effects in the production of CH4, that is, at a higher RR (Figure 2). Most experiments use concentrations below 400 mg/L. However, those experiments with higher concentrations did not result in better responses in terms of CH4 production (Figure 2).
FIGURE 2
Collecting data covering a wide range of parameters (i.e., substrate types and NPs sizes), allows more details to be compared beyond the composition of NPs. Magnetite NPs were the only composition that had enough data for a more robust evaluation of its effect on different tested parameters.
Magnetite NPs data was divided into 3 size ranges: <50 nm, between 50 and 100 nm and >100 nm (Figure 3A). The impact of magnetite NPs on CH4 production was compared by size range. NPs up to 50 nm and between 50 and 100 had better results. NPs greater than 100 nm showed worse and even inhibitory effects in CH4 production (Figure 3A). The effect of the NPs from 50 to 100 nm on CH4 production was significantly higher than the >100 nm group (Kruskal-Wallis, p = 0.0422). There was no significant difference between NPs <50 nm and between 50 and 100 nm. However, even though <50 nm had the higher results on CH4 responses (RR), NPs between 50 and 100 nm had a greater amount of data with greater increases in CH4 production than the other ranges, suggesting a more consistent effect in CH4 production (Figure 3A).
FIGURE 3
The impact of magnetite NPs on CH4 production was also evaluated as a function of the added concentration for each of the size ranges. Only NPs with dimensions up to 50 nm demonstrated a significant correlation (p < 0.05), with CH4 production, despite a relatively lower fit (r2 = 0.06324), clearly indicating the larger benefits of addition of less than 100 mg/L (Figure 3B). In other words, adding more NPs does not generate better results in CH4 production, it can actually cause the inverse effect. However, the lower line fit corroborates that it is not just the concentration of NPs that defines the positive effect in CH4 production. For NPs with dimensions between 50 and 100 nm, similar impacts on CH4 production were observed for concentrations of approximately 50 mg/L (Figure 3C).
Considering that pre-treatments can increase CH4 production (), we also evaluated the magnetite response when applied associated with and without a pre-treatment. It was possible to observe that when magnetite NPs were added with some kind of pre-treatment it had only beneficial effects (Figure 4).
FIGURE 4
It is important to highlight that the addition of NPs was not considered as a pre-treatment. Evaluating the role of NPs as an AD pre-treatment has been observed by some studies (; ) and may be worth future investigation, but it was not the goal of this study.
4 Discussion
The main compositions of NPs with better average effects on CH4 production were those of cobalt, zero valent iron and magnetite. It is worth noting that the number of experiments using magnetite NPs is much higher than for iron and cobalt. Magnetite NPs popularity and performance may be related to the diversity of effects reported for this composition, especially its driving role in DIET (; ). Magnetite is a metal oxide obtained relatively easily, most often by the process of co-precipitation or hydrothermal decomposition (). Despite being the most studied NPs, the majority of the studies that presented enough information about NPs did not get much more depth discussions about the microbiology perspective, being limited just to observations about chemical parameters (i.e., VFAs, pH, H2S variations).
Analyzing both structural and functional changes in the community as well as the chemical characteristics is essential to a better understanding of magnetite effects in AD. This highlights the importance of interdisciplinary collaborations in this kind of studies. However, few studies did connect their NPs results with the microbiologic analysis. used 8 mM of magnetite in the AD of rice plantation residues and observed that there was a modulation of the microbial community with the enrichment of the Geobacter and Methanosaeta genera, which also perform DIET, and increase of substrate degradation in addition to increasing the methanogenic activity (). applied 20 mM of magnetite into artificial wastewater with high sulfate concentration and increased CH4 production and the number of bacteria genera related to sulfate reduction and methanogenic archaea.
These results indicate the stimulation of DIET among these microorganisms and therefore add a potential tool for “H2S removal” to the possible advantages of using magnetite NPs in AD (). In addition to the modulation of the microbial community by stimulating DIET, the release of Fe+2 ions can favor the formation of iron sulfide salts, helping to mitigate the formation of H2S, which is toxic to a series of microorganisms. Increase in H2S concentrations may result in pH decrease in the system and also in high corrosion of pipes and other facilities, in addition to presenting significant risks to human health when inhaled (; ).
Even fewer studies explored both the relation between the NPs and the microbial community. , reported changes in the magnetite structure throughout the municipal waste AD process. Authors observed that not only a NPs size decrease, but also a loss of Fe+2 NPs content. The sustained release of iron from magnetite NPs stimulated the activity of methanogens without causing toxicity to the system, leading to an increase in the production of biogas by 180% and even the total CH4 percentage (). Fe+2 ions are of great importance in methanogenic metabolism, but it is noteworthy that iron ions can also be released by iron oxides such as hematite, maghemite and magnetite, depending on their crystallographic characteristics, which are determinant in the dissolution of these minerals (; ). In studies involving species of the genus Methanothermobacter, the importance of iron supply for the synthesis of a series of enzymes such as hydrogenases, dehydrogenases and reductases, in addition to ferredoxins, was observed ().
It is worth noting that merging different amounts of more than one composition of NPs might also display good improvements in CH4 yields. tested different concentrations of Ni, Co, Fe and magnetite and then combinations between these compositions in the AD of poultry waste. These authors observed that the concentrations of 4.5 mg/L of Co, 100 mg/L of Fe and 15 mg/L of magnetite increased by circa 30% the CH4 production, and significantly decreased H2S production (). Similar mixtures also promoted an increase of 23.7% in the production of biogas and a significant depletion in the production of H2S in large scale digesters (30 L) (). The benefits of NPs such as Co and Ni have been attributed to a possible supplementation of these elements as important components for some enzymatic processes for the microorganisms’ metabolism. For the Co NPs, for example, as it is necessary for synthesizing cobalamin and coenzyme B12, important parts of enzymatic complexes are involved in methanogenesis. Thus, supplementing this and other trace elements through NPs benefits metabolic improvements in AD (Zhang et al., 2009).
Depending on their concentration, smaller magnetite NPs seem to achieve a more effective result in the production of biogas (Figures 3A, B). The NPs’ surface area is inversely proportional to their average size, especially considering that most NPs usually have spherical shape (; ; Zaidi et al., 2021; Yu et al., 2022). Thus, the addition of NPs with smaller dimensions would have comparably more advantages over larger ones, in addition to potentially presenting better dispersion with less material expense in the sludge present in the reactors.
However, it was observed that, even though <50 nm NPs have the highest individual effect on CH4 production, NPs between 50 and 100 nm promote a mean larger increase in CH4 production (Figure 3A), suggesting that intermediate NPs may be more predictable and less variable impacts on biogas production. The increase of CH4 production of this size range does not have a significant correlation with its concentration, suggesting that more factors are involved in its effect on AD.
The findings that NPs concentrations below 100 mg/L with <50 nm sizes (Figure 3), suggest a possible “limit” in the concentration for the use of magnetite, that could be attributed to their probable dissolution over time, releasing Fe+2 and Fe+3 ions. This could be potentially beneficial, especially considering that Fe is of great importance in the formation of enzymes important in the metabolism of most microorganisms involved in AD. However, it should always be remembered that iron becomes toxic to most microorganisms at higher concentrations ().
As NPs between 50 and 100 nm seem to be more resistant to dissolution and, therefore, less likely to cause overdose stress, they should be preferably used in AD. The lack of statistical correlation between concentration variables and the CH4 production response for NPs between 50 and 100 nm not only suggests that there are more variables influencing this impact, but that their effect must go beyond the release of iron ions, since the high concentration could easily cause stress. Thus, it is likely that NPs in this size range have a driving influence as a stimulus to DIET rather than iron release. However, such deductions can only be confirmed with certainty from the use of analyzes of the microbial community linked to the conductivity profile of the digestate (; ).
An increase of studies in crystallographic characterization of the NPs applied to AD could be very enlightening to elucidate their effect, especially because of the existence of irregular faces in the crystals (e.g., the non-typical regular expected geometric morphologies like spherical, cuboid, etc.) that provide electronic instability in the molecular structure of the crystal. Apparently, it seems that NPs with shapes with inclusions that result in the largest contact surface would be of greater interest if the purpose of their addition were strictly the release of iron ions. However, stating that the impact of NPs on the system is solely caused by its iron release is only possible with refined characterization techniques of the nanomaterials added (i.e., analytical microscopy techniques). The crystallographic characteristics of the NPs materials used have an important hole in the resistance and hardness of these NPs. It means that depending on the crystallography of the NPs, their degradation inside the AD system may differ. It can be advantageous if the NPs benefits are related to the sustained release of some elements (i.e., Fe and Co), but it also means that some NPs compositions may persist for longer periods inside the AD than others. Magnetite, for example, has three crystallographic faces: [110], [111] and [100]. According to studies by and , the [111] face is twice as prone to dissolution due to the compact molecular arrangement of oxygen atoms, which would be more easily protonated in acidified environments. This kind of characterization was rarely observed in the studies involving NPs addition in AD ().
described that magnetite NPs with distinct surfaces, dissolution and aggregation potential presented different stability and aggregation/disaggregation behaviors according to organic matter concentrations and pH and that this also had a larger impact on particle surface charge status. This means that, depending on where and how NPs are released, their impact can vary from just being suspended particles, as an ions source, to potentially contaminants absorption. This result highlights the need for studies involving the nanotechnology application to AD. Even though a large amount of data based on the addition of magnetite NPs allowed the establishment of clear patterns, more experiments about their structure and other compositions could contribute to reach a deeper impact on all potential roles of NPs to AD.
The limited number of studies suggests a knowledge gap associated with the characterization of the changes promoted directly on the AD microbial community, but also the crystalline and chemical profiles of the NPs employed. Therefore, it is important to standardize the minimum information required in these types of research to allow the comparison, validation and reproducibility of the results described in the literature.
5 Conclusion
Here, we observed that some NPs have a direct and stimulatory effect on CH4 production, especially magnetite NPs, while other chemical compositions had inhibitory and/or opposite effects depending on the substrate, chemical composition and concentration used in the AD process. Magnetite NPs showed greater benefits with <100 nm sizes and <100 mg/L concentrations; thus these are potentially the future of Nanotechnology in AD for enhancing biogas production. In addition, the fact that the increase in the concentration and size of the NPs used does not directly result in better results in the production of CH4 has a significant impact on the cost of NPs addition in AD. The development of methods to increase CH4 production in AD by the addition of NPs is a promising strategy. Future studies must include proper characterization of the NPs studied as well as microbial community analysis for better understanding of its effects. For a more in-depth discussion on the NPs crystallographic characteristics, it would be necessary to carry analytical electron microscopy techniques like high-resolution transmission electron microscopy (HRTEM), electron energy loss spectroscopy (EELS) analysis, X-ray diffraction (XRD), and X-ray absorption spectroscopy (XANES). These techniques would allow the understanding of the size, shape and structural behavior of the NPs, as well as its possible ion releases and chemical bondings during AD.
Statements
Data availability statement
The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding authors.
Author contributions
JCC: Conceptualization, Data curation, Investigation, Methodology, Writing–original draft. ER: Data curation, Writing–original draft. IT: Writing–original draft, Methodology, Formal analysis. AE-P: Conceptualization, Funding acquisition, Writing–review and editing, Project administration, Supervision. FA: Conceptualization, Funding acquisition, Project administration, Supervision, Writing–review and editing.
Funding
The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. Financial support was provided by the Brazilian agencies CNPq, CAPES, and FAPERJ. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brasil (CAPES)—Finance Code 001. AE-P gratefully acknowledges financial support from the Swedish Energy Agency (project number P2023-00827) and the funding agency Formas (Grant number: 2021-02429). AE-P received funds from the Swedish Energy Agency (Grant number: 35624-2) at the Biogas Research Solution Center hosted by Linköping University, Sweden.
Acknowledgments
The authors acknowledge the Brazilian agencies CNPq, CAPES, FAPERJ.
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.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fnano.2024.1406344/full#supplementary-material
References
1
AbanadesS.AbbaspourH.AhmadiA.DasB.EhyaeiM. A.EsmaeilionF.et al (2022). A critical review of biogas production and usage with legislations framework across the globe. Int. J. Environ. Sci. Technol.19 (4), 3377–3400. 10.1007/s13762-021-03301-6
2
AbdelsalamE.SamerM.AttiaY.Abdel-HadiM.HassanH.BadrY. (2016). Comparison of nanoparticles effects on biogas and methane production from anaerobic digestion of cattle dung slurry. Renew. Energy87, 592–598. 10.1016/j.renene.2015.10.053
3
AbdelsalamE.SamerM.AttiaY.Abdel-HadiM.HassanH.BadrY. (2017a). Effects of Co and Ni nanoparticles on biogas and methane production from anaerobic digestion of slurry. Energy Convers. Manag.141, 108–119. 10.1016/j.enconman.2016.05.051
4
AbdelsalamE.SamerM.AttiaY.Abdel-HadiM.HassanH.BadrY. (2017b). Influence of zero valent iron nanoparticles and magnetic iron oxide nanoparticles on biogas and methane production from anaerobic digestion of manure. Energy120, 842–853. 10.1016/j.energy.2016.11.137
5
AbdelwahabT. A. M.MohantyM. K.SahooP. K.BeheraD. (2020). Application of nanoparticles for biogas production: current status and perspectives. Energy Sources, Part A Recovery, Util. Environ. Eff., 1–13. 10.1080/15567036.2020.1767730
6
AdnanI.OngM.NomanbhayS.ChewK.ShowP. (2019). Technologies for biogas upgrading to biomethane: a review. Bioengineering6 (4), 92. 10.3390/bioengineering6040092
7
AllenG. C.KirbyC.SellersR. M. (1988). The effect of the low-oxidation-state metal ion reagent tris-picolinatovanadium(II) formate on the surface morphology and composition of crystalline iron oxides. J. Chem. Soc. Faraday Trans. 1 Phys. Chem. Condens. Phases84 (1), 355–364. 10.1039/F19888400355
8
Amo-DuoduG.TettehE. K.RathilalS.ArmahE. K.AdedejiJ.ChollomM. N.et al (2021). Effect of engineered biomaterials and magnetite on wastewater treatment: biogas and kinetic evaluation. Polymers13 (24), 4323. 10.3390/polym13244323
9
AnacletoT. M.Kozlowsky-SuzukiB.BjörnA.YektaS. S.MasudaL. S. M.de OliveiraV. P.et al (2024). Methane yield response to pretreatment is dependent on substrate chemical composition: a meta-analysis on anaerobic digestion systems. Sci. Rep.14 (1), 1240–1312. 10.1038/s41598-024-51603-9
10
AnacletoT. M.Kozlowsky-SuzukiB.WilsonA. E.Enrich-PrastA. (2022). Comprehensive meta-analysis of pathways to increase biogas production in the textile industry. Energies15 (15), 5574. 10.3390/en15155574
11
AppelsL.BaeyensJ.DegrèveJ.DewilR. (2008). Principles and potential of the anaerobic digestion of waste-activated sludge. Prog. Energy Combust. Sci.34 (6), 755–781. 10.1016/j.pecs.2008.06.002
12
AtelgeM. R.KrisaD.KumarG.EskiciogluC.NguyenD. D.ChangS. W.et al (2020). Biogas production from organic waste: recent progress and perspectives. Waste Biomass Valorization11 (3), 1019–1040. 10.1007/s12649-018-00546-0
13
BaniamerianH.IsfahaniP. G.TsapekosP.Alvarado-MoralesM.ShahrokhiM.VossoughiM.et al (2019). Application of nano-structured materials in anaerobic digestion: current status and perspectives. Chemosphere229, 188–199. 10.1016/j.chemosphere.2019.04.193
14
CasalsE.BarrenaR.GarcíaA.GonzálezE.DelgadoL.Busquets‐FitéM.et al (2014). Programmed iron oxide nanoparticles disintegration in anaerobic digesters boosts biogas production. Small10 (14), 2801–2808. 10.1002/smll.201303703
15
ChenY. C. (2017). A tutorial on kernel density estimation and recent advances. Biostat. Epidemiol.1 (1), 161–187. 10.1080/24709360.2017.1396742
16
Cruz ViggiC.CasaleS.ChouchaneH.AskriR.FaziS.CherifA.et al (2019). Magnetite nanoparticles enhance the bioelectrochemical treatment of municipal sewage by facilitating the syntrophic oxidation of volatile fatty acids. J. Chem. Technol. Biotechnol.94 (10), 3134–3146. 10.1002/jctb.6120
17
CuiP.GeJ.ChenY.ZhaoY.WangS.SuH. (2022). The Fe3O4 nanoparticles-modified mycelium pellet-based anaerobic granular sludge enhanced anaerobic digestion of food waste with high salinity and organic load. Renew. Energy185, 376–385. 10.1016/j.renene.2021.12.050
18
DengL.LiuY.WangW. (2020) Biogas technology, biogas technology. Singapore: Springer Singapore. 10.1007/978-981-15-4940-3
19
FarghaliM.AndriamanohiarisoamananaF. J.AhmedM. M.KotbS.YamamotoY.IwasakiM.et al (2020). Prospects for biogas production and H2S control from the anaerobic digestion of cattle manure: the influence of microscale waste iron powder and iron oxide nanoparticles. Waste Manag.101, 141–149. 10.1016/j.wasman.2019.10.003
20
FarghaliM.AndriamanohiarisoamananaF. J.AhmedM. M.KotbS.YamashiroT.IwasakiM.et al (2019). Impacts of iron oxide and titanium dioxide nanoparticles on biogas production: hydrogen sulfide mitigation, process stability, and prospective challenges. J. Environ. Manag.240, 160–167. 10.1016/j.jenvman.2019.03.089
21
FuL.ZhouT.WangJ.YouL.LuY.YuL.et al (2019). NanoFe3O4 as solid electron shuttles to accelerate acetotrophic methanogenesis by methanosarcina barkeri. Front. Microbiol.10, 1–13. 10.3389/fmicb.2019.00388
22
GoswamiR.ChattopadhyayP.ShomeA.BanerjeeS. N.ChakrabortyA. K.MathewA. K.et al (2016). An overview of physico-chemical mechanisms of biogas production by microbial communities: a step towards sustainable waste management. 3 Biotech.6 (1), 72–12. 10.1007/s13205-016-0395-9
23
GrosserA.GrobelakA.RoratA.CourtoisP.VandenbulckeF.LemièreS.et al (2021). Effects of silver nanoparticles on performance of anaerobic digestion of sewage sludge and associated microbial communities. Renew. Energy171, 1014–1025. 10.1016/j.renene.2021.02.127
24
HammerØ.SpocovaJ. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron.4 (1). 10.26879/384
25
HassaneinA.KellerE.LansingS. (2021). Effect of metal nanoparticles in anaerobic digestion production and plant uptake from effluent fertilizer. Bioresour. Technol.321, 124455. 10.1016/j.biortech.2020.124455
26
HassaneinA.LansingS.TikekarR. (2019). Impact of metal nanoparticles on biogas production from poultry litter. Bioresour. Technol.275, 200–206. 10.1016/j.biortech.2018.12.048
27
HeS.DengQ.XianP.LiZ.TanS.LiuQ. (2019). Volatile fatty acid (VFA) and methane generation from sewage sludge and banana straw: influence of pH and two-phase anaerobic fermentation. Desalination Water Treat.152, 208–213. 10.5004/dwt.2019.23872
28
HedgesL. V.GurevitchJ.CurtisP. S. (1999). The meta-analysis of response ratios in experimental ecology. Ecology80 (4), 1150–1156. 10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2
29
HernándezS. P.ChiapperoM.RussoN.FinoD. (2011). A novel ZnO-based adsorbent for biogas purification in H2 production systems. Chem. Eng. J.176–177, 272–279. 10.1016/j.cej.2011.06.085
30
HuJ. D.ZeviY.KouX. M.XiaoJ.WangX. J.JinY. (2010). Effect of dissolved organic matter on the stability of magnetite nanoparticles under different pH and ionic strength conditions. Sci. Total Environ.408 (16), 3477–3489. 10.1016/j.scitotenv.2010.03.033
31
HuangJ.MaK.XiaX.GaoK.LuY. (2020). Biochar and magnetite promote methanogenesis during anaerobic decomposition of rice straw. Soil Biol. Biochem.143 (5), 107740–107744. 10.1016/j.soilbio.2020.107740
32
JinZ.ZhaoZ.ZhangY. (2019). Potential of direct interspecies electron transfer in synergetic enhancement of methanogenesis and sulfate removal in an up-flow anaerobic sludge blanket reactor with magnetite. Sci. Total Environ.677, 299–306. 10.1016/j.scitotenv.2019.04.372
33
JuntupallyS.BegumS.AlluS. K.NakkasunchiS.MadugulaM.AnupojuG. R. (2017). Relative evaluation of micronutrients (MN) and its respective nanoparticles (NPs) as additives for the enhanced methane generation. Bioresour. Technol.238, 290–295. 10.1016/j.biortech.2017.04.049
34
KasterA. K.GoenrichM.SeedorfH.LiesegangH.WollherrA.GottschalkG.et al (2011). More than 200 genes required for methane formation from H2 and CO2 and energy conservation are present in methanothermobacter marburgensis and methanothermobacter thermautotrophicus. Archaea2011 (1), 1–23. 10.1155/2011/973848
35
KatoS.HashimotoK.WatanabeK. (2012). Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals. Environ. Microbiol.14 (7), 1646–1654. 10.1111/j.1462-2920.2011.02611.x
36
LagoeiroL. E. (1998). Transformation of magnetite to hematite and its influence on the dissolution of iron oxide minerals. J. Metamorph. Geol.16 (3), 415–423. 10.1111/j.1525-1314.1998.00144.x
37
LiuX.DuM.LuQ.HeD.SongK.YangQ.et al (2021). How does chitosan affect methane production in anaerobic digestion?Environ. Sci. Technol.55 (23), 15843–15852. 10.1021/acs.est.1c04693
38
LovleyD. R. (2017). Syntrophy goes electric: direct interspecies electron transfer. Annu. Rev. Microbiol.71, 643–664. 10.1146/annurev-micro-030117-020420
39
MadsenM.Holm-NielsenJ. B.EsbensenK. H. (2011). Monitoring of anaerobic digestion processes: a review perspective. Renew. Sustain. Energy Rev.15 (6), 3141–3155. 10.1016/j.rser.2011.04.026
40
MotulskyH. J.BrownR. E. (2006). Detecting outliers when fitting data with nonlinear regression - a new method based on robust nonlinear regression and the false discovery rate. BMC Bioinforma.7, 123–220. 10.1186/1471-2105-7-123
41
PageM. J.MoherD.BossuytP. M.BoutronI.HoffmannT. C.MulrowC. D.et al (2021). PRISMA 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews. BMJ372, n160. 10.1136/bmj.n160
42
ParkJ. H.KangH. J.ParkK. H.ParkH. D. (2018). Direct interspecies electron transfer via conductive materials: a perspective for anaerobic digestion applications. Bioresour. Technol.254, 300–311. 10.1016/j.biortech.2018.01.095
43
PatinvohR. J.OsadolorO. A.ChandoliasK.Sárvári HorváthI.TaherzadehM. J. (2017). Innovative pretreatment strategies for biogas production. Bioresour. Technol.224, 13–24. 10.1016/j.biortech.2016.11.083
44
ReddyL. H.AriasJ. L.NicolasJ.CouvreurP. (2012). Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chem. Rev.112 (11), 5818–5878. 10.1021/cr300068p
45
RotaruA. E.ShresthaP. M.LiuF.ShresthaM.ShresthaD.EmbreeM.et al (2014). A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ. Sci.7 (1), 408–415. 10.1039/c3ee42189a
46
ScarlatN.DallemandJ. F.FahlF. (2018). Biogas: developments and perspectives in europe. Renew. Energy129, 457–472. 10.1016/j.renene.2018.03.006
47
SchnürerA.JarvisÅ. (2018) Microbiology of the biogas process. SLU. Uppsala, Sweden: Swedish University of Agricultural Sciences.
48
SuC.ZhengP.LinX.ChenW.LiX.ChenQ.et al (2019). Influence of amoxicillin after pre-treatment on the extracellular polymeric substances and microbial community of anaerobic granular sludge. Bioresour. Technol.276, 81–90. 10.1016/j.biortech.2018.12.104
49
TedescoS.HurstG.ImtiazA.RatovaM.ToshevaL.KellyP. (2020). TiO2 supported natural zeolites as biogas enhancers through photocatalytic pre-treatment of Miscanthus x giganteous crops. Energy205, 117954. 10.1016/j.energy.2020.117954
50
TruongD. H.EghbalM. A.HindmarshW.RothS. H.O'BrienP. J. (2006). Molecular mechanisms of hydrogen sulfide toxicity. Drug Metab. Rev.38 (4), 733–744. 10.1080/03602530600959607
51
UysalY.MutB. (2020). Biogas and methane production efficiency of sewage sludge supplemented with conductive materials. Int. J. Glob. Warming20 (4), 353–373. 10.1504/IJGW.2020.107153
52
Van HouwelingenH. C.ArendsL. R.StijnenT. (2002). Advanced methods in meta-analysis: multivariate approach and meta-regression. Statistics Med.21 (4), 589–624. 10.1002/sim.1040
53
WangQ.XiaC.AlagumalaiK.Thanh Nhi LeT.YuanY.KhademiT.et al (2023). Biogas generation from biomass as a cleaner alternative towards a circular bioeconomy: artificial intelligence, challenges, and future insights. Fuel333 (P2), 126456. 10.1016/j.fuel.2022.126456
54
XuF.LiY.GeX.YangL.LiY. (2018). Anaerobic digestion of food waste – challenges and opportunities. Bioresour. Technol.247, 1047–1058. 10.1016/j.biortech.2017.09.020
55
YamazakiT. (2020). Reductive dissolution of biogenic magnetite. Earth, Planets Space72 (1), 150. 10.1186/s40623-020-01290-3
56
YuJ.LiuJ.Senthil KumarP.WeiY.ZhouM.VoD. V. N.et al (2022). Promotion of methane production by magnetite via increasing acetogenesis revealed by metagenome-assembled genomes. Bioresour. Technol.345, 126521. 10.1016/j.biortech.2021.126521
57
ZaidiA. A.KhanS. Z.AlmohamadiH.MahmoudE. R. I.NaseerM. N. (2021). Nanoparticles synergistic effect with various substrate pretreatment and their comparison on biogas production from algae waste. Bull. Chem. React. Eng. Catal.16 (2), 374–382. 10.9767/bcrec.16.2.10637.374-382
58
ZhangY.RodionovD. A.GelfandM. S.GladyshevV. N. (2009). Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genomics10, 78. 10.1186/1471-2164-10-78
59
ZiganshinaE. E.BulyninaS. S.ZiganshinA. M. (2022). Impact of granular activated carbon on anaerobic process and microbial community structure during mesophilic and thermophilic anaerobic digestion of chicken manure. Sustain. Switz.14 (1), 447. 10.3390/su14010447
Summary
Keywords
biogas, nanoparticles, meta-analysis, biotechnology, methane
Citation
Castro JC, Resende E, Taveira I, Enrich-Prast A and Abreu F (2024) Nanotechnology boosts the production of clean energy via nanoparticle addition in anaerobic digestion. Front. Nanotechnol. 6:1406344. doi: 10.3389/fnano.2024.1406344
Received
24 March 2024
Accepted
22 April 2024
Published
16 May 2024
Volume
6 - 2024
Edited by
Sasanka Deka, University of Delhi, India
Reviewed by
Avishek Banik, Colorado State University, United States
Brij Kishore, CSIR-CMERI Center of Excellence for Farm Machinery, India
Updates
Copyright
© 2024 Castro, Resende, Taveira, Enrich-Prast and Abreu.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: F. Abreu, fernandaaabreu@micro.ufrj.br; A. Enrich-Prast, alex.enrich.prast@liu.se
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