Journal Article

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

Adam, Panagiotis S., McKay, Luke J., Chen, Lin-Xing, Ghozlane, Amine, de Oliveira, Valéria Maia, Inskeep, William P., Li, Wen-Jun, Andersen, Gary L., Hallam, Steven J., Muyzer, Gerard, Sierra-García, Isabel Natalia, Sieber, Christian M. K., Banfield, Jillian F., Letourneur, Quentin, Borrel, Guillaume, Gribaldo, Simonetta

2019

Overview

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. A search for methyl-coenzyme M reductase complex (MCR) and MCR-like homologues—which govern methane and short-chain alkane metabolism—across publicly available metagenomes reveals that these metabolic pathways are widespread and diverse in archaea, and may in some organisms be linked to alkane and/or fatty acid oxidation.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/181/757 / 631/326/26/2142 / 631/326/26/2523 / 631/326/26/2524 / 631/326/26/2527 / Alkanes - chemistry / Alkanes - metabolism / Archaea - classification / Archaea - genetics / Archaea - growth & development / Archaea - metabolism / Bacteriology / BASIC BIOLOGICAL SCIENCES / Biodiversity / Biomedical and Life Sciences / Candidatus Verstraetearchaeota / Coenzyme M / DNA, Archaeal / Energy conservation / Genomes / Infectious Diseases / Life Sciences / Medical Microbiology / Metabolism / Metagenome / Methane / Methane - chemistry / Methane - metabolism / Methanogenesis / Methanogenic bacteria / Microbiology / Microbiology and Parasitology / Oxidation / Oxidation-Reduction / Parasitology / Phylogeny / Populations and Evolution / Reductase / Systematics, Phylogenetics and taxonomy / Virology