Dataset Information

Sulfur and Methane-Oxidizing Microbial Community in a Terrestrial Mud Volcano Revealed by Metagenomics.

ABSTRACT: Mud volcanoes are prominent geological structures where fluids and gases from the deep subsurface are discharged along a fracture network in tectonically active regions. Microbial communities responsible for sulfur and methane cycling and organic transformation in terrestrial mud volcanoes remain poorly characterized. Using a metagenomics approach, we analyzed the microbial community of bubbling fluids retrieved from an active mud volcano in eastern Crimea. The microbial community was dominated by chemolithoautotrophic Campylobacterota and Gammaproteobacteria, which are capable of sulfur oxidation coupled to aerobic and anaerobic respiration. Methane oxidation could be enabled by aerobic Methylococcales bacteria and anaerobic methanotrophic archaea (ANME), while methanogens were nearly absent. The ANME community was dominated by a novel species of Ca. Methanoperedenaceae that lacked nitrate reductase and probably couple methane oxidation to the reduction of metal oxides. Analysis of two Ca. Bathyarchaeota genomes revealed the lack of mcr genes and predicted that they could grow on fatty acids, sugars, and proteinaceous substrates performing fermentation. Thermophilic sulfate reducers indigenous to the deep subsurface, Thermodesulfovibrionales (Nitrospirae) and Ca. Desulforudis (Firmicutes), were found in minor amounts. Overall, the results obtained suggest that reduced compounds delivered from the deep subsurface support the development of autotrophic microorganisms using various electron acceptors for respiration.

SUBMITTER: Mardanov AV

PROVIDER: S-EPMC7565565 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Sulfur and Methane-Oxidizing Microbial Community in a Terrestrial Mud Volcano Revealed by Metagenomics.

Mardanov Andrey V AV Kadnikov Vitaly V VV Beletsky Alexey V AV Ravin Nikolai V NV

Microorganisms 20200831 9

Mud volcanoes are prominent geological structures where fluids and gases from the deep subsurface are discharged along a fracture network in tectonically active regions. Microbial communities responsible for sulfur and methane cycling and organic transformation in terrestrial mud volcanoes remain poorly characterized. Using a metagenomics approach, we analyzed the microbial community of bubbling fluids retrieved from an active mud volcano in eastern Crimea. The microbial community was dominated ...[more]

PMID: 32878336

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Project description:Terrestrial mud volcanoes (MVs) are an important natural source of methane emission. The role of microbial processes in methane cycling and organic transformation in such environments remains largely unexplored. In this study, we aim to uncover functional potentials and community assemblages across geochemical transitions in a ferruginous, sulfate-depleted MV of eastern Taiwan. Geochemical profiles combined with 16S rRNA gene abundances indicated that anaerobic oxidation of methane (AOM) mediated by ANME-2a group coincided with iron/manganese reduction by Desulfuromonadales at shallow depths deprived of sulfate. The activity of AOM was stimulated either by methane alone or by methane and a range of electron acceptors, such as sulfate, ferrihydrite, and artificial humic acid. Metagenomic analyses revealed that functional genes for AOM and metal reduction were more abundant at shallow intervals. In particular, genes encoding pili expression and electron transport through multi-heme cytochromes were prevalent, suggesting potential intercellular interactions for electron transport involved in AOM. For comparison, genes responsible for methanogenesis and degradation of chitin and plant-derived molecules were more abundant at depth. The gene distribution combined with the enhanced proportions of 16S rRNA genes related to methanogens and heterotrophs, and geochemical characteristics suggest that particulate organic matter was degraded into various organic entities that could further fuel in situ methanogenesis. Finally, genes responsible for aerobic methane oxidation were more abundant in the bubbling pool and near-surface sediments. These methane oxidizers account for the ultimate attenuation of methane discharge into the atmosphere. Overall, our results demonstrated that various community members were compartmentalized into stratified niches along geochemical gradients. These community members form a metabolic network that cascades the carbon transformation from the upstream degradation of recalcitrant organic carbon with fermentative production of labile organic entities and methane to downstream methane oxidation and metal reduction near the surface. Such a metabolic architecture enables effective methane removal under ferruginous, sulfate-depleted conditions in terrestrial MVs.

Project description:In recent years, the externalization of electrons as part of respiratory metabolic processes has been discovered in many different bacteria and some archaea. Microbial extracellular electron transfer (EET) plays an important role in many anoxic natural or engineered ecosystems. In this study, an anaerobic methane-converting microbial community was investigated with regard to its potential to perform EET. At this point, it is not well-known if or how EET confers a competitive advantage to certain species in methane-converting communities. EET was investigated in a two-chamber electrochemical system, sparged with methane and with an applied potential of +400 mV versus standard hydrogen electrode. A biofilm developed on the working electrode and stable low-density current was produced, confirming that EET indeed did occur. The appearance and presence of redox centers at -140 to -160 mV and at -230 mV in the biofilm was confirmed by cyclic voltammetry scans. Metagenomic analysis and fluorescence in situ hybridization of the biofilm showed that the anaerobic methanotroph 'Candidatus Methanoperedens BLZ2' was a significant member of the biofilm community, but its relative abundance did not increase compared to the inoculum. On the contrary, the relative abundance of other members of the microbial community significantly increased (up to 720-fold, 7.2% of mapped reads), placing these microorganisms among the dominant species in the bioanode community. This group included Zoogloea sp., Dechloromonas sp., two members of the Bacteroidetes phylum, and the spirochete Leptonema sp. Genes encoding proteins putatively involved in EET were identified in Zoogloea sp., Dechloromonas sp. and one member of the Bacteroidetes phylum. We suggest that instead of methane, alternative carbon sources such as acetate were the substrate for EET. Hence, EET in a methane-driven chemolithoautotrophic microbial community seems a complex process in which interactions within the microbial community are driving extracellular electron transfer to the electrode.

Dataset Information

Sulfur and Methane-Oxidizing Microbial Community in a Terrestrial Mud Volcano Revealed by Metagenomics.

Publications

Sulfur and Methane-Oxidizing Microbial Community in a Terrestrial Mud Volcano Revealed by Metagenomics.

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