Evolutionary diversification of methanotrophic ANME-1 archaea and their expansive virome

Rafael Laso-Pérez (1) , Fabai Wu (2, 3, 4) , Antoine Crémière (4) , Daan R Speth (4) , John S Magyar (4) , Kehan Zhao (2) , Mart Krupovic (5) , Victoria J Orphan (4)

1 Universität Bremen
2 ZJU - ZJU-Hangzhou Global Scientific and Technological Innovation Center
3 Zhejiang University
4 CALTECH - California Institute of Technology
5 Virologie des archées - Archaeal Virology

‘Candidatus Methanophagales’ (ANME-1) is an order-level clade of archaea responsible for anaerobic methane oxidation in deep-sea sediments. The diversity, ecology and evolution of ANME-1 remain poorly understood. In this study, we use metagenomics on deep-sea hydrothermal samples to expand ANME-1 diversity and uncover the effect of virus–host dynamics. Phylogenetic analyses reveal a deep-branching, thermophilic family, ‘ Candidatus Methanospirareceae’, closely related to short-chain alkane oxidizers. Global phylogeny and near-complete genomes show that hydrogen metabolism within ANME-1 is an ancient trait that was vertically inherited but differentially lost during lineage diversification. Metagenomics also uncovered 16 undescribed virus families so far exclusively targeting ANME-1 archaea, showing unique structural and replicative signatures. The expansive ANME-1 virome contains a metabolic gene repertoire that can influence host ecology and evolution through virus-mediated gene displacement. Our results suggest an evolutionary continuum between anaerobic methane and short-chain alkane oxidizers and underscore the effects of viruses on the dynamics and evolution of methane-driven ecosystems.

Domaines: Sciences du Vivant [q-bio]

Rafael Laso-Pérez, Fabai Wu, Antoine Crémière, Daan R Speth, John S Magyar, et al.. Evolutionary diversification of methanotrophic ANME-1 archaea and their expansive virome. Nature Microbiology, 2023, 8 (2), pp.231-245. ⟨10.1038/s41564-022-01297-4⟩. ⟨pasteur-03976007⟩