Panagiotis S. Adam, Guillaume Borrel, Wen-Jun Li, Steven J. Hallam, William P. Inskeep, Luke J. McKay, Gary L. Andersen, Simonetta Gribaldo, Quentin Letourneur, Amine Ghozlane, Isabel N. Sierra-Garcia, Gerard Muyzer, Valéria Maia de Oliveira, Lin-Xing Chen, Jillian F. Banfield, Christian M. K. Sieber, Biologie Evolutive de la Cellule Microbienne - Evolutionary Biology of the Microbial Cell, Institut Pasteur [Paris] (IP), Université Paris Diderot - Paris 7 (UPD7), Montana State University (MSU), Lawrence Berkeley National Laboratory [Berkeley] (LBNL), Universidade Estadual de Campinas = University of Campinas (UNICAMP), Hub Bioinformatique et Biostatistique - Bioinformatics and Biostatistics HUB, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Sun Yat-Sen University [Guangzhou] (SYSU), University of British Columbia (UBC), University of Amsterdam [Amsterdam] (UvA), 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)., ANR-16-CE02-0005,Arch-Evol,Approches phylogenomiques pour étudier l'origine et évolution des Archées(2016), European Project: 322551,EC:FP7:ERC,ERC-2012-ADG_20120314,PARASOL(2013), Institut Pasteur [Paris], University of Campinas [Campinas] (UNICAMP), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Sun Yat-Sen University (SYSU), and Freshwater and Marine Ecology (IBED, FNWI)
International audience; 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.