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

Laso-Pérez, Rafael; Wu, Fabai; Crémière, Antoine; Speth, Daan R.; Magyar, John S.; Zhao, Kehan; Krupovic, Mart; Orphan, Victoria J.

doi:10.1038/s41564-022-01297-4

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

Journal Article · Wed Jan 18 23:00:00 EST 2023 · Nature Microbiology

DOI:https://doi.org/10.1038/s41564-022-01297-4· OSTI ID:2470710

^[1]; ^[2]; ^[3]; Speth, Daan R. ^[4]; ^[3]; Zhao, Kehan ^[5]; ^[6]; ^[3]

Centro Nacional de Biotecnología (CNB-CSIC), Madrid (Spain); Univ. of Bremen (Germany)
ZJU-Hangzhou Global Scientific and Technological Innovation Center (China); Zhejiang Univ. (China); Donghai Laboratory (China); California Institute of Technology (CalTech), Pasadena, CA (United States)
California Institute of Technology (CalTech), Pasadena, CA (United States)
Max-Planck Institute for Marine Microbiology, Bremen (Germany); California Institute of Technology (CalTech), Pasadena, CA (United States)
ZJU-Hangzhou Global Scientific and Technological Innovation Center (China)
Paris Cité University (France); Centre National de la Recherche Scientifique (CNRS) (France)

'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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0020373

OSTI ID:: 2470710

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 2 Vol. 8; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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