Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane
Terrestrial mud volcanoes (TMVs) are important natural sources of methane emission. The microorganisms inhabiting these environments remain largely unknown. We studied the phylogenetic composition and metabolic potential of the prokaryotic communities of TMVs located in the Taman Peninsula, Russia,...
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2021-09-01
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author | Alexander Y. Merkel Nikolay A. Chernyh Nikolai V. Pimenov Elizaveta A. Bonch-Osmolovskaya Alexander I. Slobodkin |
author_facet | Alexander Y. Merkel Nikolay A. Chernyh Nikolai V. Pimenov Elizaveta A. Bonch-Osmolovskaya Alexander I. Slobodkin |
author_sort | Alexander Y. Merkel |
collection | DOAJ |
description | Terrestrial mud volcanoes (TMVs) are important natural sources of methane emission. The microorganisms inhabiting these environments remain largely unknown. We studied the phylogenetic composition and metabolic potential of the prokaryotic communities of TMVs located in the Taman Peninsula, Russia, using a metagenomic approach. One of the examined sites harbored a unique community with a high abundance of anaerobic methane-oxidizing archaea belonging to ANME-3 group (39% of all 16S rRNA gene reads). The high number of ANME-3 archaea was confirmed by qPCR, while the process of anaerobic methane oxidation was demonstrated by radioisotopic experiments. We recovered metagenome-assembled genomes (MAGs) of archaeal and bacterial community members and analyzed their metabolic capabilities. The ANME-3 MAG contained a complete set of genes for methanogenesis as well as of ribosomal RNA and did not encode proteins involved in dissimilatory nitrate or sulfate reduction. The presence of multiheme <i>c</i>-type cytochromes suggests that ANME-3 can couple methane oxidation with the reduction of metal oxides or with the interspecies electron transfer to a bacterial partner. The bacterial members of the community were mainly represented by autotrophic, nitrate-reducing, sulfur-oxidizing bacteria, as well as by fermentative microorganisms. This study extends the current knowledge of the phylogenetic and metabolic diversity of prokaryotes in TMVs and provides a first insight into the genomic features of ANME-3 archaea. |
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spelling | doaj.art-43862132822643ba91de9b30a53476f52023-11-22T13:56:25ZengMDPI AGLife2075-17292021-09-0111995310.3390/life11090953Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of MethaneAlexander Y. Merkel0Nikolay A. Chernyh1Nikolai V. Pimenov2Elizaveta A. Bonch-Osmolovskaya3Alexander I. Slobodkin4Research Center of Biotechnology, Winogradsky Institute of Microbiology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaResearch Center of Biotechnology, Winogradsky Institute of Microbiology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaResearch Center of Biotechnology, Winogradsky Institute of Microbiology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaResearch Center of Biotechnology, Winogradsky Institute of Microbiology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaResearch Center of Biotechnology, Winogradsky Institute of Microbiology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaTerrestrial mud volcanoes (TMVs) are important natural sources of methane emission. The microorganisms inhabiting these environments remain largely unknown. We studied the phylogenetic composition and metabolic potential of the prokaryotic communities of TMVs located in the Taman Peninsula, Russia, using a metagenomic approach. One of the examined sites harbored a unique community with a high abundance of anaerobic methane-oxidizing archaea belonging to ANME-3 group (39% of all 16S rRNA gene reads). The high number of ANME-3 archaea was confirmed by qPCR, while the process of anaerobic methane oxidation was demonstrated by radioisotopic experiments. We recovered metagenome-assembled genomes (MAGs) of archaeal and bacterial community members and analyzed their metabolic capabilities. The ANME-3 MAG contained a complete set of genes for methanogenesis as well as of ribosomal RNA and did not encode proteins involved in dissimilatory nitrate or sulfate reduction. The presence of multiheme <i>c</i>-type cytochromes suggests that ANME-3 can couple methane oxidation with the reduction of metal oxides or with the interspecies electron transfer to a bacterial partner. The bacterial members of the community were mainly represented by autotrophic, nitrate-reducing, sulfur-oxidizing bacteria, as well as by fermentative microorganisms. This study extends the current knowledge of the phylogenetic and metabolic diversity of prokaryotes in TMVs and provides a first insight into the genomic features of ANME-3 archaea.https://www.mdpi.com/2075-1729/11/9/953mud volcanomicrobial communitiesarchaeadiversitymetagenomemethane |
spellingShingle | Alexander Y. Merkel Nikolay A. Chernyh Nikolai V. Pimenov Elizaveta A. Bonch-Osmolovskaya Alexander I. Slobodkin Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane Life mud volcano microbial communities archaea diversity metagenome methane |
title | Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane |
title_full | Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane |
title_fullStr | Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane |
title_full_unstemmed | Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane |
title_short | Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane |
title_sort | diversity and metabolic potential of the terrestrial mud volcano microbial community with a high abundance of archaea mediating the anaerobic oxidation of methane |
topic | mud volcano microbial communities archaea diversity metagenome methane |
url | https://www.mdpi.com/2075-1729/11/9/953 |
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