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Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea

Journal Article · · Nature Microbiology
 [1];  [2];  [3];  [4];  [5];  [6];  [1];  [1];  [4];  [7];  [8];  [9];  [5];  [3];  [4];  [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)
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.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1545147
Journal Information:
Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 4 Vol. 4; ISSN 2058-5276
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (16)

Methyl (Alkyl)-Coenzyme M Reductases: Nickel F-430-Containing Enzymes Involved in Anaerobic Methane Formation and in Anaerobic Oxidation of Methane or of Short Chain Alkanes journal April 2019
Insights into the ecological roles and evolution of methyl-coenzyme M reductase-containing hot spring Archaea journal October 2019
The Syntrophy hypothesis for the origin of eukaryotes revisited journal April 2020
More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV journal December 2020
New Insights into the Ecology and Physiology of Methanomassiliicoccales from Terrestrial and Aquatic Environments journal December 2020
Microbial community composition and functional potential in Bothnian Sea sediments is linked to Fe and S dynamics and the quality of organic matter journal January 2020
Metal-dependent anaerobic methane oxidation in marine sediment: Insights from marine settings and other systems journal June 2019
Methylamine-specific methyltransferase paralogs in Methanosarcina are functionally distinct despite frequent gene conversion journal May 2019
Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota journal March 2019
An archaeal origin of the Wood–Ljungdahl H4MPT branch and the emergence of bacterial methylotrophy journal August 2019
Methylotrophic methanogens everywhere — physiology and ecology of novel players in global methane cycling journal December 2019
First evidence for cold-adapted anaerobic oxidation of methane in deep sediments of thermokarst lakes journal March 2019
Anaerobic Degradation of Non-Methane Alkanes by “ Candidatus Methanoliparia” in Hydrocarbon Seeps of the Gulf of Mexico journal August 2019
Genomic and transcriptomic insights into methanogenesis potential of novel methanogens from mangrove sediments journal June 2020
Functional interactions between posttranslationally modified amino acids of methyl-coenzyme M reductase in Methanosarcina acetivorans journal February 2020
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