Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane.
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ABSTRACT:
SUBMITTER: Merkel AY
PROVIDER: S-EPMC8470020 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description: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.
| S-EPMC7565565 | biostudies-literature
Project description:Submarine mud volcanoes are formed by expulsions of mud, fluids, and gases from deeply buried subsurface sources. They are highly reduced benthic habitats and often associated with intensive methane seepage. In this study, the microbial diversity and community structure in methane-rich sediments of the Haakon Mosby Mud Volcano (HMMV) were investigated by comparative sequence analysis of 16S rRNA genes and fluorescence in situ hybridization. In the active volcano center, which has a diameter of about 500 m, the main methane-consuming process was bacterial aerobic oxidation. In this zone, aerobic methanotrophs belonging to three bacterial clades closely affiliated with Methylobacter and Methylophaga species accounted for 56%+/-8% of total cells. In sediments below Beggiatoa mats encircling the center of the HMMV, methanotrophic archaea of the ANME-3 clade dominated the zone of anaerobic methane oxidation. ANME-3 archaea form cell aggregates mostly associated with sulfate-reducing bacteria of the Desulfobulbus (DBB) branch. These ANME-3/DBB aggregates were highly abundant and accounted for up to 94%+/-2% of total microbial biomass at 2 to 3 cm below the surface. ANME-3/DBB aggregates could be further enriched by flow cytometry to identify their phylogenetic relationships. At the outer rim of the mud volcano, the seafloor was colonized by tubeworms (Siboglinidae, formerly known as Pogonophora). Here, both aerobic and anaerobic methane oxidizers were found, however, in lower abundances. The level of microbial diversity at this site was higher than that at the central and Beggiatoa species-covered part of the HMMV. Analysis of methyl-coenzyme M-reductase alpha subunit (mcrA) genes showed a strong dominance of a novel lineage, mcrA group f, which could be assigned to ANME-3 archaea. Our results further support the hypothesis of Niemann et al. (54), that high methane availability and different fluid flow regimens at the HMMV provide distinct niches for aerobic and anaerobic methanotrophs.
| S-EPMC1907091 | biostudies-literature
Project description:Anaerobic oxidation of methane (AOM) is crucial for controlling the emission of this potent greenhouse gas to the atmosphere. Nitrite-, nitrate-, and sulfate-dependent methane oxidation is well-documented, but AOM coupled to the reduction of oxidized metals has so far been demonstrated only in environmental samples. Here, using a freshwater enrichment culture, we show that archaea of the order Methanosarcinales, related to "Candidatus Methanoperedens nitroreducens," couple the reduction of environmentally relevant forms of Fe3+ and Mn4+ to the oxidation of methane. We obtained an enrichment culture of these archaea under anaerobic, nitrate-reducing conditions with a continuous supply of methane. Via batch incubations using [13C]methane, we demonstrated that soluble ferric iron (Fe3+, as Fe-citrate) and nanoparticulate forms of Fe3+ and Mn4+ supported methane-oxidizing activity. CO2 and ferrous iron (Fe2+) were produced in stoichiometric amounts. Our study connects the previous finding of iron-dependent AOM to microorganisms detected in numerous habitats worldwide. Consequently, it enables a better understanding of the interaction between the biogeochemical cycles of iron and methane.
| S-EPMC5111651 | biostudies-literature
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.
| S-EPMC5673622 | biostudies-literature
Project description:The anaerobic oxidation of methane (AOM) with sulfate controls the emission of the greenhouse gas methane from the ocean floor. AOM is performed by microbial consortia of archaea (ANME) associated with partners related to sulfate-reducing bacteria. In vitro enrichments of AOM were so far only successful at temperatures ?25?°C; however, energy gain for growth by AOM with sulfate is in principle also possible at higher temperatures. Sequences of 16S rRNA genes and core lipids characteristic for ANME as well as hints of in situ AOM activity were indeed reported for geothermally heated marine environments, yet no direct evidence for thermophilic growth of marine ANME consortia was obtained to date. To study possible thermophilic AOM, we investigated hydrothermally influenced sediment from the Guaymas Basin. In vitro incubations showed activity of sulfate-dependent methane oxidation between 5 and 70?°C with an apparent optimum between 45 and 60?°C. AOM was absent at temperatures ?75?°C. Long-term enrichment of AOM was fastest at 50?°C, yielding a 13-fold increase of methane-dependent sulfate reduction within 250 days, equivalent to an apparent doubling time of 68 days. The enrichments were dominated by novel ANME-1 consortia, mostly associated with bacterial partners of the deltaproteobacterial HotSeep-1 cluster, a deeply branching phylogenetic group previously found in a butane-amended 60?°C-enrichment culture of Guaymas sediments. The closest relatives (Desulfurella spp.; Hippea maritima) are moderately thermophilic sulfur reducers. Results indicate that AOM and ANME archaea could be of biogeochemical relevance not only in cold to moderate but also in hot marine habitats.
| S-EPMC3223311 | biostudies-literature
Project description:Microbial life is widespread in the terrestrial subsurface and present down to several kilometers depth, but the energy sources that fuel metabolism in deep oligotrophic and anoxic environments remain unclear. In the deep crystalline bedrock of the Fennoscandian Shield at Olkiluoto, Finland, opposing gradients of abiotic methane and ancient seawater-derived sulfate create a terrestrial sulfate-methane transition zone (SMTZ). We used chemical and isotopic data coupled to genome-resolved metaproteogenomics to demonstrate active life and, for the first time, provide direct evidence of active anaerobic oxidation of methane (AOM) in a deep terrestrial bedrock. Proteins from Methanoperedens (formerly ANME-2d) are readily identifiable despite the low abundance (≤1%) of this genus and confirm the occurrence of AOM. This finding is supported by 13C-depleted dissolved inorganic carbon. Proteins from Desulfocapsaceae and Desulfurivibrionaceae, in addition to 34S-enriched sulfate, suggest that these organisms use inorganic sulfur compounds as both electron donor and acceptor. Zerovalent sulfur in the groundwater may derive from abiotic rock interactions, or from a non-obligate syntrophy with Methanoperedens, potentially linking methane and sulfur cycles in Olkiluoto groundwater. Finally, putative episymbionts from the candidate phyla radiation (CPR) and DPANN archaea represented a significant diversity in the groundwater (26/84 genomes) with roles in sulfur and carbon cycling. Our results highlight AOM and sulfur disproportionation as active metabolisms and show that methane and sulfur fuel microbial activity in the deep terrestrial subsurface.
| S-EPMC9123182 | biostudies-literature
Project description:Cold seeps and hydrothermal vents deliver large amounts of methane and other gaseous alkanes into marine surface sediments. Consortia of archaea and partner bacteria thrive on the oxidation of these alkanes and its coupling to sulfate reduction. The inherently slow growth of the involved organisms and the lack of pure cultures have impeded the understanding of the molecular mechanisms of archaeal alkane degradation. Here, using hydrothermal sediments of the Guaymas Basin (Gulf of California) and ethane as the substrate, we cultured microbial consortia of a novel anaerobic ethane oxidizer, "Candidatus Ethanoperedens thermophilum" (GoM-Arc1 clade), and its partner bacterium "Candidatus Desulfofervidus auxilii," previously known from methane-oxidizing consortia. The sulfate reduction activity of the culture doubled within one week, indicating a much faster growth than in any other alkane-oxidizing archaea described before. The dominance of a single archaeal phylotype in this culture allowed retrieval of a closed genome of "Ca. Ethanoperedens," a sister genus of the recently reported ethane oxidizer "Candidatus Argoarchaeum." The metagenome-assembled genome of "Ca. Ethanoperedens" encoded a complete methanogenesis pathway including a methyl-coenzyme M reductase (MCR) that is highly divergent from those of methanogens and methanotrophs. Combined substrate and metabolite analysis showed ethane as the sole growth substrate and production of ethyl-coenzyme M as the activation product. Stable isotope probing demonstrated that the enzymatic mechanism of ethane oxidation in "Ca. Ethanoperedens" is fully reversible; thus, its enzymatic machinery has potential for the biotechnological development of microbial ethane production from carbon dioxide.IMPORTANCE In the seabed, gaseous alkanes are oxidized by syntrophic microbial consortia that thereby reduce fluxes of these compounds into the water column. Because of the immense quantities of seabed alkane fluxes, these consortia are key catalysts of the global carbon cycle. Due to their obligate syntrophic lifestyle, the physiology of alkane-degrading archaea remains poorly understood. We have now cultivated a thermophilic, relatively fast-growing ethane oxidizer in partnership with a sulfate-reducing bacterium known to aid in methane oxidation and have retrieved the first complete genome of a short-chain alkane-degrading archaeon. This will greatly enhance the understanding of nonmethane alkane activation by noncanonical methyl-coenzyme M reductase enzymes and provide insights into additional metabolic steps and the mechanisms underlying syntrophic partnerships. Ultimately, this knowledge could lead to the biotechnological development of alkanogenic microorganisms to support the carbon neutrality of industrial processes.
| S-EPMC7175092 | biostudies-literature
Project description:Anaerobic methanotrophic archaea have recently been identified in anoxic marine sediments, but have not yet been recovered in pure culture. Physiological studies on freshly collected samples containing archaea and their sulfate-reducing syntrophic partners have been conducted, but sample availability and viability can limit the scope of these experiments. To better study microbial anaerobic methane oxidation, we developed a novel continuous-flow anaerobic methane incubation system (AMIS) that simulates the majority of in situ conditions and supports the metabolism and growth of anaerobic methanotrophic archaea. We incubated sediments collected from within and outside a methane cold seep in Monterey Canyon, Calif., for 24 weeks on the AMIS system. Anaerobic methane oxidation was measured in all sediments after incubation on AMIS, and quantitative molecular techniques verified the increases in methane-oxidizing archaeal populations in both seep and nonseep sediments. Our results demonstrate that the AMIS system stimulated the maintenance and growth of anaerobic methanotrophic archaea, and possibly their syntrophic, sulfate-reducing partners. Our data demonstrate the utility of combining physiological and molecular techniques to quantify the growth and metabolic activity of anaerobic microbial consortia. Further experiments with the AMIS system should provide a better understanding of the biological mechanisms of methane oxidation in anoxic marine environments. The AMIS may also enable the enrichment, purification, and isolation of methanotrophic archaea as pure cultures or defined syntrophic consortia.
| S-EPMC194967 | biostudies-literature
Project description:Uncultured sequence reads
| PRJNA415004 | ENA
Project description:Terrestrial mud volcanism represents the prominent surface geological feature, where fluids and hydrocarbons are discharged along deeply rooted structures in tectonically active regimes. Terrestrial mud volcanoes (MVs) directly emit the major gas phase, methane, into the atmosphere, making them important sources of greenhouse gases over geological time. Quantification of methane emission would require detailed insights into the capacity and efficiency of microbial metabolisms either consuming or producing methane in the subsurface, and establishment of the linkage between these methane-related metabolisms and other microbial or abiotic processes. Here we conducted geochemical, microbiological and genetic analyses of sediments, gases, and pore and surface fluids to characterize fluid processes, community assemblages, functions and activities in a methane-emitting MV of southwestern Taiwan. Multiple lines of evidence suggest that aerobic/anaerobic methane oxidation, sulfate reduction and methanogenesis are active and compartmentalized into discrete, stratified niches, resembling those in marine settings. Surface evaporation and oxidation of sulfide minerals are required to account for the enhanced levels of sulfate that fuels subsurface sulfate reduction and anaerobic methanotrophy. Methane flux generated by in situ methanogenesis appears to alter the isotopic compositions and abundances of thermogenic methane migrating from deep sources, and to exceed the capacity of microbial consumption. This metabolic stratification is sustained by chemical disequilibria induced by the mixing between upward, anoxic, methane-rich fluids and downward, oxic, sulfate-rich fluids.
| S-EPMC3504961 | biostudies-literature