Evolutionary diversification of methanotrophic ANME-1 archaea and their expansive virome
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Abstract
‘ 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.
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- Authors
- Laso-Pérez, R., Wu, F., Crémière, A., Speth, D. R., Magyar, J. S., Zhao, K., Krupovic, M., & Orphan, V. J.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- California Institute of Technology (US)
- Corresponding author
- Laso-Pérez, Rafael
- Wu, Fabai
- Orphan, Victoria J.
- ORCID
- Venue
- Nature Microbiology
- Published
- 2023-01-19
- Volume
- 8
- Issue
- 2
- Pages
- 231-245
- ISSN
- 2058-5276 (ISSN-L)
- PMC
- PMC9894754
- OpenAlex
- W4317501562
- Cited by
- 68
- References
- 4
- Citations by year
- 2026: 17 · 2025: 23 · 2024: 19 · 2023: 8 · 2022: 1
- FWCI
- 5.78
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Nature Microbiology (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by)
- HAL (submittedVersion, cc-by)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion, other-oa)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by-nc-nd)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- U.S. Department of Energy (DESC0020373)
- Dalio Foundation
- Center for Dark Energy Biosphere Investigations
- Schmidt Ocean Institute
- Deutsche Forschungsgemeinschaft (390741603, EXC-2077, EXC-2077390741603)
- Agence Nationale de la Recherche (ANR-20-CE20-0009)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (019.162LW.037)
- Universidad Autónoma de Baja California
- NOMIS Stiftung
- Office of Science (DESC0020373)
- University of California, Davis
- Biological and Environmental Research (#DE-SC0020373)
- FP7 International Cooperation
- Topics
- Physical Sciences › Environmental Science › Environmental Chemistry › Methane Hydrates and Related Phenomena
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Keywords
- anaerobic oxidation of methane, host-virus interaction, hydrogen metabolism, archaeal evolution, thermophilic archaea
- MeSH terms
- Virome, Alkanes, Anaerobiosis, Archaea, Methane, Phylogeny, Ecosystem, Geologic Sediments
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