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

Guillaume Borrel (1) , Panagiotis S Adam (1, 2) , Luke J Mckay (3) , Lin-Xing Chen (4) , Isabel Natalia Sierra-García (5) , Christian M K Sieber (4) , Quentin Letourneur (6) , Amine Ghozlane (6) , Gary Andersen (4) , Wen-Jun Li (7) , Steven J Hallam (8) , Gerard Muyzer (9) , Valéria Maia de Oliveira (5) , William P Inskeep (3) , Jillian F Banfield (4) , Simonetta Gribaldo (1)

1 Biologie Evolutive de la Cellule Microbienne - Evolutionary Biology of the Microbial Cell
2 UPD7 - Université Paris Diderot - Paris 7
3 MSU - Montana State University
4 LBNL - Lawrence Berkeley National Laboratory [Berkeley]
5 UNICAMP - Universidade Estadual de Campinas = University of Campinas
6 Hub Bioinformatique et Biostatistique - Bioinformatics and Biostatistics HUB
7 SYSU - Sun Yat-sen University [Guangzhou]
8 UBC - University of British Columbia
9 UvA - University of Amsterdam [Amsterdam] = Universiteit van Amsterdam

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.

Domaines: Bactériologie; Systématique, phylogénie et taxonomie; Evolution [q-bio.PE]

Guillaume Borrel, Panagiotis S Adam, Luke J Mckay, Lin-Xing Chen, Isabel Natalia Sierra-García, et al.. Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. Nature Microbiology, 2019, ⟨10.1038/s41564-019-0363-3⟩. ⟨pasteur-02059013⟩