Methanogenesis is an ancient metabolism of key ecological relevance, with direct impact on the evolution of Earth’s climate. Recent results suggest that the diversity of methane metabolisms and their derivations have probably been vastly underestimated. Here, 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.
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We thank R. Thauer for feedback on an earlier version of the manuscript. G.B. acknowledges support from the Institut Pasteur through a Roux-Cantarini fellowship. P.S.A. is supported by a PhD fellowship from Paris Diderot University and by funds from the PhD Programme ‘Frontières du Vivant (FdV)-Programme Bettencourt’. S.G. acknowledges funding from the French National Agency for Research Grant ArchEvol (No. ANR-16-CE02-0005-01). This work used the computational and storage services (TARS cluster) provided by the IT department at Institut Pasteur, Paris. S.J.H. acknowledges support from the US Department of Energy (DOE) JGI supported by the Office of Science of US DOE Contract No. DE-AC02–05CH11231, the Natural Sciences and Engineering Research Council (NSERC) of Canada, Genome British Columbia, Genome Canada, Canada Foundation for Innovation (CFI) and the Tula Foundation. I.N.S.-G. and V.M.d.O. are grateful to São Paulo Research Foundation—FAPESP (process Nos. 2011/14501-6 and 2013/20436-8) and Petrobras for financial support and to N. Gray and I. Head from the School of Civil Engineering and Geosciences at Newcastle University for lab facilities. W-J.L. was supported by Key Projects of Ministry of Science and Technology (MOST) (Nos. 2013DFA31980 and 2015FY110100). G.M. was supported by the ERC Advanced Grant PARASOL (No. 322551). L.J.M. appreciates funding from the NASA Postdoctoral Programme through the NASA Astrobiology Institute and W.P.I. was supported by the Montana Agricultural Experiment Station (Project No. 911300).
The authors declare no competing interests.
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Supplementary Discussion, Supplementary References, Legends for Supplementary Tables, Supplementary Table 2, Supplementary Table 4, Supplementary Table 5, and Supplementary Figures 1–13.
Presence/absence of genes involved in specific substrate utilization, energy metabolism, cofactor biosynthesis, secretion, sulfate assimilation, N2 fixation, dissimilatory reduction of inorganic compounds and motility. Pathways and systems are subdivided into different spreadsheets. In each spreadsheet and for each metagenome-assembled genome, protein accession numbers with the same colour indicate co-localized genes.
Occurrence in archaea of 38 genes previously suggested to be methanogenesis markers.
Genomes used to build the archaea reference tree (Fig. 1). The first spreadsheet shows the number of genomes available and selected for the phylogeny, and the second spreadsheet gives the NCBI accession numbers (if any) of the selected genomes.
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