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Title: 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:
ORCiD logo [1];  [2]; ORCiD logo [3];  [4];  [5];  [6];  [1];  [1];  [4]; ORCiD logo [7]; ORCiD logo [8]; ORCiD logo [9];  [5]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [1]
  1. Institut Pasteur, Paris (France)
  2. Institut Pasteur, Paris (France); Université Paris Diderot, Paris (France)
  3. Montana State Univ., Bozeman, MT (United States)
  4. Univ. of California, Berkeley, CA (United States)
  5. Univ. of Campinas (UNICAMP), Sao Paulo (Brazil)
  6. Univ. of California, Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. Sun Yat-Sen Univ., Guangzhou, (China)
  8. Univ. of British Columbia, Vancouver, BC (Canada)
  9. Univ. of Amsterdam (Netherlands)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (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. 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., and Gribaldo, Simonetta. Mon . "Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea". United States. doi:10.1038/s41564-019-0363-3.
@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 = {2019},
month = {3}
}

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Works referenced in this record:

Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics
journal, October 2015


Higher-level classification of the Archaea: evolution of methanogenesis and methanogens
journal, January 2005

  • Bapteste, Éric; Brochier, Céline; Boucher, Yan
  • Archaea, Vol. 1, Issue 5
  • DOI: 10.1155/2005/859728

Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis
journal, May 2017


Molecular mechanism of energy conservation in polysulfide respiration
journal, June 2008

  • Jormakka, Mika; Yokoyama, Ken; Yano, Takahiro
  • Nature Structural & Molecular Biology, Vol. 15, Issue 7
  • DOI: 10.1038/nsmb.1434

The genome of Syntrophus aciditrophicus: Life at the thermodynamic limit of microbial growth
journal, April 2007

  • McInerney, M. J.; Rohlin, L.; Mouttaki, H.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 18
  • DOI: 10.1073/pnas.0610456104

Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota
journal, March 2019


Role of syntrophic microbial communities in high-rate methanogenic bioreactors
journal, July 2012

  • Stams, Alfons J. M.; Sousa, Diana Z.; Kleerebezem, Robbert
  • Water Science and Technology, Vol. 66, Issue 2
  • DOI: 10.2166/wst.2012.192

PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating
journal, June 2009


The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review
journal, January 2008

  • Demirel, Burak; Scherer, Paul
  • Reviews in Environmental Science and Bio/Technology, Vol. 7, Issue 2
  • DOI: 10.1007/s11157-008-9131-1

Genomic Insights into Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation
journal, October 2012


Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction
journal, January 2016

  • Seitz, Kiley W.; Lazar, Cassandre S.; Hinrichs, Kai-Uwe
  • The ISME Journal, Vol. 10, Issue 7
  • DOI: 10.1038/ismej.2015.233

Early bioenergetic evolution
journal, July 2013

  • Sousa, Filipa L.; Thiergart, Thorsten; Landan, Giddy
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1622
  • DOI: 10.1098/rstb.2013.0088

Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era
journal, March 2006

  • Ueno, Yuichiro; Yamada, Keita; Yoshida, Naohiro
  • Nature, Vol. 440, Issue 7083
  • DOI: 10.1038/nature04584

Computing the Internode Certainty and Related Measures from Partial Gene Trees
journal, February 2016

  • Kobert, Kassian; Salichos, Leonidas; Rokas, Antonis
  • Molecular Biology and Evolution, Vol. 33, Issue 6
  • DOI: 10.1093/molbev/msw040

The prokaryotic Mo/W-bisPGD enzymes family: A catalytic workhorse in bioenergetic
journal, August 2013

  • Grimaldi, Stéphane; Schoepp-Cothenet, Barbara; Ceccaldi, Pierre
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9
  • DOI: 10.1016/j.bbabio.2013.01.011

Reverse Methanogenesis and Respiration in Methanotrophic Archaea
journal, January 2017

  • Timmers, Peer H. A.; Welte, Cornelia U.; Koehorst, Jasper J.
  • Archaea, Vol. 2017
  • DOI: 10.1155/2017/1654237

Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis
journal, March 2013

  • Sarmiento, F.; Mrazek, J.; Whitman, W. B.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 12
  • DOI: 10.1073/pnas.1220225110

metaSPAdes: a new versatile metagenomic assembler
journal, March 2017

  • Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton
  • Genome Research, Vol. 27, Issue 5
  • DOI: 10.1101/gr.213959.116

Archaebiotics: Proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease
journal, October 2013

  • Brugère, Jean-François; Borrel, Guillaume; Gaci, Nadia
  • Gut Microbes, Vol. 5, Issue 1
  • DOI: 10.4161/gmic.26749

Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life
journal, August 2017


MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015


Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


MacSyFinder: A Program to Mine Genomes for Molecular Systems with an Application to CRISPR-Cas Systems
journal, October 2014


Single cell activity reveals direct electron transfer in methanotrophic consortia
journal, September 2015

  • McGlynn, Shawn E.; Chadwick, Grayson L.; Kempes, Christopher P.
  • Nature, Vol. 526, Issue 7574
  • DOI: 10.1038/nature15512

MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets
journal, October 2015


RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


Metagenomes from two microbial consortia associated with Santa Barbara seep oil
journal, December 2014


A Metagenomics-Based Metabolic Model of Nitrate-Dependent Anaerobic Oxidation of Methane by Methanoperedens-Like Archaea
journal, December 2015


Characterization of a second methylene tetrahydromethanopterin dehydrogenase from Methylobacterium extorquens AM1: Dehydrogenase from M. extorquens AM1
journal, June 2000


Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics
journal, September 2004


CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Methane formation from long-chain alkanes by anaerobic microorganisms
journal, September 1999

  • Zengler, Karsten; Richnow, Hans H.; Rosselló-Mora, Ramon
  • Nature, Vol. 401, Issue 6750
  • DOI: 10.1038/45777

The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea
journal, October 2016


MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014

  • Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
  • Molecular Biology and Evolution, Vol. 32, Issue 1
  • DOI: 10.1093/molbev/msu300

The RAST Server: Rapid Annotations using Subsystems Technology
journal, January 2008

  • Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A.
  • BMC Genomics, Vol. 9, Issue 1, Article No. 75
  • DOI: 10.1186/1471-2164-9-75

The physiology and habitat of the last universal common ancestor
journal, July 2016


SyntTax: a web server linking synteny to prokaryotic taxonomy
journal, January 2013


Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen
journal, March 2016

  • Nobu, Masaru Konishi; Narihiro, Takashi; Kuroda, Kyohei
  • The ISME Journal, Vol. 10, Issue 10
  • DOI: 10.1038/ismej.2016.33

CDD: NCBI's conserved domain database
journal, November 2014

  • Marchler-Bauer, Aron; Derbyshire, Myra K.; Gonzales, Noreen R.
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1221

IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments
journal, August 2017


Elucidating the Process of Activation of Methyl-Coenzyme M Reductase
journal, April 2014

  • Prakash, D.; Wu, Y.; Suh, S. -J.
  • Journal of Bacteriology, Vol. 196, Issue 13
  • DOI: 10.1128/JB.01658-14

Binning metagenomic contigs by coverage and composition
journal, September 2014

  • Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino
  • Nature Methods, Vol. 11, Issue 11
  • DOI: 10.1038/nmeth.3103

Thermophilic archaea activate butane via alkyl-coenzyme M formation
journal, October 2016

  • Laso-Pérez, Rafael; Wegener, Gunter; Knittel, Katrin
  • Nature, Vol. 539, Issue 7629
  • DOI: 10.1038/nature20152

Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group
journal, February 2010


Life and the Evolution of Earth's Atmosphere
journal, May 2002


The growing tree of Archaea: new perspectives on their diversity, evolution and ecology
journal, August 2017

  • Adam, Panagiotis S.; Borrel, Guillaume; Brochier-Armanet, Céline
  • The ISME Journal, Vol. 11, Issue 11
  • DOI: 10.1038/ismej.2017.122

Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota
journal, October 2016


PhyloSift: phylogenetic analysis of genomes and metagenomes
journal, January 2014

  • Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.243

Methanogenesis and the Wood–Ljungdahl Pathway: An Ancient, Versatile, and Fragile Association
journal, May 2016

  • Borrel, Guillaume; Adam, Panagiotis S.; Gribaldo, Simonetta
  • Genome Biology and Evolution, Vol. 8, Issue 6
  • DOI: 10.1093/gbe/evw114

Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria
journal, October 2015

  • Wegener, Gunter; Krukenberg, Viola; Riedel, Dietmar
  • Nature, Vol. 526, Issue 7574
  • DOI: 10.1038/nature15733

Energy Metabolism during Anaerobic Methane Oxidation in ANME Archaea
journal, January 2017


The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus
journal, November 1997

  • Klenk, Hans-Peter; Clayton, Rebecca A.; Tomb, Jean-Francois
  • Nature, Vol. 390, Issue 6658
  • DOI: 10.1038/37052

Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic Archaea
journal, September 2017

  • Nayak, Dipti D.; Mahanta, Nilkamal; Mitchell, Douglas A.
  • eLife, Vol. 6
  • DOI: 10.7554/eLife.29218

Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments
journal, August 2017


Phylogenomic Data Support a Seventh Order of Methylotrophic Methanogens and Provide Insights into the Evolution of Methanogenesis
journal, August 2013

  • Borrel, Guillaume; O’Toole, Paul W.; Harris, Hugh M. B.
  • Genome Biology and Evolution, Vol. 5, Issue 10
  • DOI: 10.1093/gbe/evt128

The two-domain tree of life is linked to a new root for the Archaea
journal, May 2015

  • Raymann, Kasie; Brochier-Armanet, Céline; Gribaldo, Simonetta
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 21
  • DOI: 10.1073/pnas.1420858112

Influence of biodegradation on crude oil acidity and carboxylic acid composition
journal, November 2000


Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes
journal, January 2018

  • Adam, Panagiotis S.; Borrel, Guillaume; Gribaldo, Simonetta
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 6
  • DOI: 10.1073/pnas.1716667115