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PreprintCited by 68Methane Hydrates and Related PhenomenaMicrobial Community Ecology and PhysiologyMicrobial metabolism and enzyme function

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Evolutionary Diversification of Methanotrophic Ca . Methanophagales (ANME-1) and Their Expansive Virome

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Laso-Pérez, Rafael, Wu, Fabai, Crémière, Antoine, Speth, Daan R., Magyar, John S., Krupovic, Mart, Orphan, Victoria J.·2022·Nature Microbiology
DOI 10.1101/2022.07.04.498658PMC PMC9894754

Preprint — published as 10.1038/s41564-022-01297-4 · Paper page

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Abstract

‘ Candidatus Methanophagales’ (ANME-1) is a major order-level clade of archaea responsible for methane removal in deep-sea sediments through the anaerobic oxidation of methane. Yet the extent of their diversity and factors which drive their dynamics and evolution remain poorly understood. Here, by sampling hydrothermal rocks and sediments, we expand their phylogenetic diversity and characterize a new deep-branching, thermophilic ANME-1 family, ‘ Candidatus Methanospirareceae’ (ANME-1c). They are phylogenetically closest to the short-chain-alkane oxidizers ‘ Candidatus Syntrophoarchaeales’ and ‘ Candidatus Alkanophagales’, and encode ancestral features including a methyl coenzyme M reductase chaperone McrD and a hydrogenase complex. Global phylogeny and near-complete genomes clarified that the debated hydrogen metabolism within ANME-1 is an ancient trait that was vertically inherited but differentially lost during lineage diversification. Our expanded genomic and metagenomic sampling allowed the discovery of viruses constituting 3 new orders and 16 new families that so far are exclusive to ANME-1 hosts. These viruses represent 4 major archaeal virus assemblages, characterized by tailless icosahedral, head-tailed, rod-shaped, and spindle-shaped virions, but display unique structural and replicative signatures. Exemplified by the analyses of thymidylate synthases that unveiled a virus-mediated ancestral process of host gene displacement, this expansive ANME-1 virome carries a large gene repertoire that can influence their hosts across different timescales. Our study thus puts forth an emerging evolutionary continuum between anaerobic methane and short-chain-alkane oxidizers and opens doors for exploring the impacts of viruses on the dynamics and evolution of the anaerobic methane-driven ecosystems.

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Metadata

Authors
Laso-Pérez, R., Wu, F., Crémière, A., Speth, D. R., Magyar, J. S., 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
Publisher
openRxiv
Published
2022-07-04
Volume
8
Issue
2
Pages
231-245
ISSN
2058-5276 (ISSN-L)
DOI
10.1101/2022.07.04.498658
PMC
PMC9894754
OpenAlex
W4317501562
Cited by
68
References
1
Citations by year
2026: 17 · 2025: 23 · 2024: 19 · 2023: 8 · 2022: 1
FWCI
5.78
Type
journal article
Language
en
Open access
Licence
cc-by
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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