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,...

Full description

Bibliographic Details
Main Authors: Alexander Y. Merkel, Nikolay A. Chernyh, Nikolai V. Pimenov, Elizaveta A. Bonch-Osmolovskaya, Alexander I. Slobodkin
Format: Article
Language:English
Published: MDPI AG 2021-09-01
Series:Life
Subjects:
Online Access:https://www.mdpi.com/2075-1729/11/9/953
_version_ 1797518434742829056
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.
first_indexed 2024-03-10T07:29:49Z
format Article
id doaj.art-43862132822643ba91de9b30a53476f5
institution Directory Open Access Journal
issn 2075-1729
language English
last_indexed 2024-03-10T07:29:49Z
publishDate 2021-09-01
publisher MDPI AG
record_format Article
series Life
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
work_keys_str_mv AT alexanderymerkel diversityandmetabolicpotentialoftheterrestrialmudvolcanomicrobialcommunitywithahighabundanceofarchaeamediatingtheanaerobicoxidationofmethane
AT nikolayachernyh diversityandmetabolicpotentialoftheterrestrialmudvolcanomicrobialcommunitywithahighabundanceofarchaeamediatingtheanaerobicoxidationofmethane
AT nikolaivpimenov diversityandmetabolicpotentialoftheterrestrialmudvolcanomicrobialcommunitywithahighabundanceofarchaeamediatingtheanaerobicoxidationofmethane
AT elizavetaabonchosmolovskaya diversityandmetabolicpotentialoftheterrestrialmudvolcanomicrobialcommunitywithahighabundanceofarchaeamediatingtheanaerobicoxidationofmethane
AT alexanderislobodkin diversityandmetabolicpotentialoftheterrestrialmudvolcanomicrobialcommunitywithahighabundanceofarchaeamediatingtheanaerobicoxidationofmethane