Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea
Abstract
Methanogenesis is an archaic metabolism of key ecological relevance, with direct impact on the evolution of Earth's climate. Recent findings indicate that the diversity of methane metabolisms and their derivations have probably been vastly underestimated. In this work, by probing thousands of publicly available metagenomes for homologues of methyl-coenzyme M reductase complex (MCR), we have obtained ten metagenome-assembled genomes (MAGs) belonging to potential methanogenic, anaerobic methanotrophic and short-chain alkane-oxidizing archaea. Five of these MAGs represent under-sampled (Verstraetearchaeota, Methanonatronarchaeia, ANME-1 and GoM-Arc1) or previously genomically undescribed (ANME-2c) archaeal lineages. The remaining five MAGs correspond to lineages that are only distantly related to previously known methanogens and span the entire archaeal phylogeny. Comprehensive comparative annotation substantially expands the metabolic diversity and energy conservation systems of MCR-bearing archaea. It also suggests the potential existence of a yet uncharacterized type of methanogenesis linked to short-chain alkane/fatty acid oxidation in a previously undescribed class of archaea ('Candidatus Methanoliparia'). We redefine a common core of marker genes specific to methanogenic, anaerobic methanotrophic and short-chain alkane-oxidizing archaea, and propose a possible scenario for the evolutionary and functional transitions that led to the emergence of such metabolic diversity.
- Authors:
-
[1];
[3];
[7];
[8];
[9];
[3];
[4];
[1]
- Institut Pasteur, Paris (France)
- Institut Pasteur, Paris (France); Université Paris Diderot, Paris (France)
- Montana State Univ., Bozeman, MT (United States)
- Univ. of California, Berkeley, CA (United States)
- Univ. of Campinas (UNICAMP), Sao Paulo (Brazil)
- Univ. of California, Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Sun Yat-Sen Univ., Guangzhou, (China)
- Univ. of British Columbia, Vancouver, BC (Canada)
- Univ. of Amsterdam (Netherlands)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1545147
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Microbiology
- Additional Journal Information:
- Journal Volume: 4; Journal Issue: 4; Journal ID: ISSN 2058-5276
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Borrel, Guillaume, Adam, Panagiotis S., McKay, Luke J., Chen, Lin-Xing, Sierra-García, Isabel Natalia, Sieber, Christian M. K., Letourneur, Quentin, Ghozlane, Amine, Andersen, Gary L., Li, Wen-Jun, Hallam, Steven J., Muyzer, Gerard, de Oliveira, Valéria Maia, Inskeep, William P., Banfield, Jillian F., and Gribaldo, Simonetta. Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. United States: N. p., 2019.
Web. doi:10.1038/s41564-019-0363-3.
Borrel, Guillaume, Adam, Panagiotis S., McKay, Luke J., Chen, Lin-Xing, Sierra-García, Isabel Natalia, Sieber, Christian M. K., Letourneur, Quentin, Ghozlane, Amine, Andersen, Gary L., Li, Wen-Jun, Hallam, Steven J., Muyzer, Gerard, de Oliveira, Valéria Maia, Inskeep, William P., Banfield, Jillian F., & Gribaldo, Simonetta. Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. United States. https://doi.org/10.1038/s41564-019-0363-3
Borrel, Guillaume, Adam, Panagiotis S., McKay, Luke J., Chen, Lin-Xing, Sierra-García, Isabel Natalia, Sieber, Christian M. K., Letourneur, Quentin, Ghozlane, Amine, Andersen, Gary L., Li, Wen-Jun, Hallam, Steven J., Muyzer, Gerard, de Oliveira, Valéria Maia, Inskeep, William P., Banfield, Jillian F., and Gribaldo, Simonetta. Mon .
"Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea". United States. https://doi.org/10.1038/s41564-019-0363-3. https://www.osti.gov/servlets/purl/1545147.
@article{osti_1545147,
title = {Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea},
author = {Borrel, Guillaume and Adam, Panagiotis S. and McKay, Luke J. and Chen, Lin-Xing and Sierra-García, Isabel Natalia and Sieber, Christian M. K. and Letourneur, Quentin and Ghozlane, Amine and Andersen, Gary L. and Li, Wen-Jun and Hallam, Steven J. and Muyzer, Gerard and de Oliveira, Valéria Maia and Inskeep, William P. and Banfield, Jillian F. and Gribaldo, Simonetta},
abstractNote = {Methanogenesis is an archaic metabolism of key ecological relevance, with direct impact on the evolution of Earth's climate. Recent findings indicate that the diversity of methane metabolisms and their derivations have probably been vastly underestimated. In this work, by probing thousands of publicly available metagenomes for homologues of methyl-coenzyme M reductase complex (MCR), we have obtained ten metagenome-assembled genomes (MAGs) belonging to potential methanogenic, anaerobic methanotrophic and short-chain alkane-oxidizing archaea. Five of these MAGs represent under-sampled (Verstraetearchaeota, Methanonatronarchaeia, ANME-1 and GoM-Arc1) or previously genomically undescribed (ANME-2c) archaeal lineages. The remaining five MAGs correspond to lineages that are only distantly related to previously known methanogens and span the entire archaeal phylogeny. Comprehensive comparative annotation substantially expands the metabolic diversity and energy conservation systems of MCR-bearing archaea. It also suggests the potential existence of a yet uncharacterized type of methanogenesis linked to short-chain alkane/fatty acid oxidation in a previously undescribed class of archaea ('Candidatus Methanoliparia'). We redefine a common core of marker genes specific to methanogenic, anaerobic methanotrophic and short-chain alkane-oxidizing archaea, and propose a possible scenario for the evolutionary and functional transitions that led to the emergence of such metabolic diversity.},
doi = {10.1038/s41564-019-0363-3},
journal = {Nature Microbiology},
number = 4,
volume = 4,
place = {United States},
year = {Mon Mar 04 00:00:00 EST 2019},
month = {Mon Mar 04 00:00:00 EST 2019}
}
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