Syntrophy and Interspecies Electron Transfer in Methanogenic Microbial Communities

Ножевникова, А. Н.; Russkova, Yu. I.; Litti, Yu. V.; Parshina, Sofiya N.; Zhuravleva, Elena A.; Никитина, А. А.

doi:10.1134/s0026261720020101

Cited by 75 publications

(39 citation statements)

References 86 publications

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“…Recently, DIET is being increasingly mentioned in the context of anaerobic digestion [ 10 , 106 ]. The microbial community fed with ethanol and dominated by the Methanotrix species exhibited an elevated abundance of the bacterial pilA gene and the methanogenic sludge showed a higher conductivity.…”

Section: Discussionmentioning

confidence: 99%

“…The essence of the syntrophic interactions is interspecies electron transfer (IET) making the entire syntrophic metabolism efficient and thermodynamically favorable. IET can occur indirectly, mediated by hydrogen and formate (IIET), or directly (DIET) via contact between the microorganisms [ 7 – 10 ]. The metabolic pathways utilized for syntrophic oxidation of common non-gaseous products of acidogenesis include beta-oxidation for butyrate; the methylmalonyl-CoA pathway recognized in Syntrophobacter [ 11 , 12 ] or the dismutation pathway recognized in Smithella propionica for propionate [ 13 ]; the Wood–Ljungdahl pathway for acetate; the pathway of ethanol oxidation recognized in the genera Pelobacter and Desulfovibrio in the absence of other electron acceptors [ 14 ]; the lactate oxidation recognized in Desulfovibrio in the absence of sulfate [ 9 , 15 ].…”

Section: Introductionmentioning

confidence: 99%

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Evaluation of acidogenesis products’ effect on biogas production performed with metagenomics and isotopic approaches

Detman

Bucha

Treu

et al. 2021

Biotechnol Biofuels

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Background During the acetogenic step of anaerobic digestion, the products of acidogenesis are oxidized to substrates for methanogenesis: hydrogen, carbon dioxide and acetate. Acetogenesis and methanogenesis are highly interconnected processes due to the syntrophic associations between acetogenic bacteria and hydrogenotrophic methanogens, allowing the whole process to become thermodynamically favorable. The aim of this study is to determine the influence of the dominant acidic products on the metabolic pathways of methane formation and to find a core microbiome and substrate-specific species in a mixed biogas-producing system. Results Four methane-producing microbial communities were fed with artificial media having one dominant component, respectively, lactate, butyrate, propionate and acetate, for 896 days in 3.5-L Up-flow Anaerobic Sludge Blanket (UASB) bioreactors. All the microbial communities showed moderately different methane production and utilization of the substrates. Analyses of stable carbon isotope composition of the fermentation gas and the substrates showed differences in average values of δ13C(CH4) and δ13C(CO2) revealing that acetate and lactate strongly favored the acetotrophic pathway, while butyrate and propionate favored the hydrogenotrophic pathway of methane formation. Genome-centric metagenomic analysis recovered 234 Metagenome Assembled Genomes (MAGs), including 31 archaeal and 203 bacterial species, mostly unknown and uncultivable. MAGs accounted for 54%–67% of the entire microbial community (depending on the bioreactor) and evidenced that the microbiome is extremely complex in terms of the number of species. The core microbiome was composed of Methanothrix soehngenii (the most abundant), Methanoculleus sp., unknown Bacteroidales and Spirochaetaceae. Relative abundance analysis of all the samples revealed microbes having substrate preferences. Substrate-specific species were mostly unknown and not predominant in the microbial communities. Conclusions In this experimental system, the dominant fermentation products subjected to methanogenesis moderately modified the final effect of bioreactor performance. At the molecular level, a different contribution of acetotrophic and hydrogenotrophic pathways for methane production, a very high level of new species recovered, and a moderate variability in microbial composition depending on substrate availability were evidenced. Propionate was not a factor ceasing methane production. All these findings are relevant because lactate, acetate, propionate and butyrate are the universal products of acidogenesis, regardless of feedstock.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Evaluation of acidogenesis products’ effect on biogas production performed with metagenomics and isotopic approaches

Detman

Bucha

Treu

et al. 2021

Biotechnol Biofuels

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“…In Hodarchaeia, both coenzymes might be re-oxidised by the encoded thiol:fumarate reductase which catalyses the reduction of fumarate, with CoB and CoM as electron donors, to succinate and heterodisulfide CoM [25]. Alternatively electrons could be shuttled to a syntrophic partner via extracellular electron transfer mediated by hydrogen, formate, or acetate [26]. A symbiotic relationship would also help to complement the amino acid needs of Hodarchaeia and Jordarchaeia, which lack genes encoding the biosynthesis of the amino acids proline, tyrosine, and phenylalanine, and additionally alanine biosynthesis genes are missing in Jordarchaeia (Table S9).…”

Section: Core Metabolism and Electron Transportmentioning

confidence: 99%

Recoding enhances the metabolic capabilities of two novel methylotrophic Asgardarchaeota lineages

Sun

Evans

Gagen

et al. 2021

Preprint

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Asgardarchaeota have been proposed as the closest living relatives to eukaryotes, and a total of 72 metagenome-assembled genomes (MAGs) representing six primary lineages in this archaeal phylum have thus far been described. These organisms are predicted to be fermentative organoheterotrophs contributing to carbon cycling in sediment ecosystems. Here, we double the genomic catalogue of Asgardarchaeota by obtaining 71 MAGs from a range of habitats around the globe, including deep subsurface, shallow lake, and geothermal spring sediments. Phylogenomic inferences followed by taxonomic rank normalisation confirmed previously established Asgardarchaeota classes and revealed four novel lineages, two of which were consistently recovered as monophyletic classes. We therefore propose the names Candidatus Hodarchaeia class nov. and Cand. Jordarchaeia class nov., derived from the gods Hod and Jord in Norse mythology. Metabolic inference suggests that both novel classes represent methylotrophic acetogens, encoding the transfer of methyl groups, such as methylated amines, to coenzyme M with acetate as the end product in remnants of a methanogen-derived core metabolism. This inferred mode of energy conservation is predicted to be enhanced by genetic code expansions, i.e. recoding, allowing the incorporation of the rare 21st and 22nd amino acids selenocysteine (Sec) and pyrrolysine (Pyl). We found Sec recoding in Jordarchaeia and all other Asgardarchaeota classes, which likely benefit from increased catalytic activities of Sec-containing enzymes. Pyl recoding on the other hand is restricted to Hodarchaeia in the Asgardarchaeota, making it the first reported non-methanogenic lineage with an inferred complete Pyl machinery, likely providing this class with an efficient mechanism for methylamine utilisation. Furthermore, we identified enzymes for the biosynthesis of ester-type lipids, characteristic of Bacteria and Eukaryotes, in both novel classes, supporting the hypothesis that mixed ether-ester lipids are a shared feature among Asgardarchaeota.

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“…This implies that once the utilization of H 2 is slow due to the environmental conditions, the consumption and degradation of propionate and butyrate by acetogens would also be slow, thereby leading to the accumulation of these acids which eventually causes digestion failure. Similar constraint exists for formate and therefore any impediment in the consumption of these mediators (H 2 and formate) causes an accumulation of VFA which in turn obstructs the syntrophic process due to the inhibitory effect of VFA on microbial cells (NOZHEVNIKOVA et al, 2020).…”

Section: Introductionmentioning

confidence: 98%

“…Previously published reviews have generally focussed on the means by which biochar can promote AD including the alleviation of inhibition by VFA and ammonia; adsorption of heavy metals; increasing methane production or improving biogas and digestate quality (MASEBINU et al, 2019, Codignole LUZ et al, 2018Qiu et al, 2019;CHIAPPERO et al, 2020). Additionally, there are other reviews on mechanisms of IET, mediation of DIET by various modes, i.e., membrane-bound electron transport proteins, conductive pili and abiotic conductive materials, and microbiology of IET (NOZHEVNIKOVA et al, 2020;ZHANG & ZANG, 2019;ZHAO et al, 2020). However, none of these reviews provides a comprehensive description and analysis of biochar properties in relation to syntrophic metabolism in AD and the biochar engineering strategies to obtain desired properties for enhanced syntrophy and AD efficiency.…”

Section: Introductionmentioning

confidence: 99%

Syntrophic interactions in anaerobic digestion: how biochar properties affect them?

Johnravindar

Patria

Lee

et al. 2021

Sustainable Environment

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Biochar as a biomass derived, low cost, carbon conductive material is considered as an important supplement in the anaerobic digestion (AD) of organic matter. It functions as an electrical grid to allow direct electron transfer from fatty acid oxidizers to methanogenic archaea, thereby promoting syntophy between various microbial groups and leading to efficient methanogenesis. Specific properties of biochar play an important role in promoting syntrophic interactions in AD. As a physical indicator, surface area, porosity, particle size and surface texture of biochar play an important role in governing microbial attachment and enrichment on biochar. This influences the microbial degradation of fatty acids and their subsequent conversion to methane by methanogens. Chemical properties such as the presence of hydrophobic functional groups, molecular nature and redox active groups on biochar surface promote interaction between biochar and microorganisms and provide an increased degree of electron transfer between the attached microorganisms. The above characteristics depend on feedstock and pyrolysis conditions used for biochar production. Unlike previous reviews, herein the desired physical and chemical properties of biochar that promote syntrophy in AD and the factors that influence them have been discussed in detail. Furthermore, engineering of biochar properties by various activation methods to harness favourable characteristics of biochar as an effective AD additive is described. Such a comprehensive account would be useful for engineering efficient biochar-mediated digestions with enhanced syntrophy and overall AD performance.

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Syntrophy and Interspecies Electron Transfer in Methanogenic Microbial Communities

Cited by 75 publications

References 86 publications

Evaluation of acidogenesis products’ effect on biogas production performed with metagenomics and isotopic approaches

Evaluation of acidogenesis products’ effect on biogas production performed with metagenomics and isotopic approaches

Recoding enhances the metabolic capabilities of two novel methylotrophic Asgardarchaeota lineages

Syntrophic interactions in anaerobic digestion: how biochar properties affect them?

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