PreprintCited by 108Bacteriophages and microbial interactionsPlant and Fungal Interactions ResearchAquaculture disease management and microbiota

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Plankton-infecting relatives of herpesviruses clarify the evolutionary trajectory of giant viruses

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Gaïa, Morgan, Meng, Lingjie, Pelletier, Eric, Forterre, Patrick, Vanni, Chiara, Fernandez-Guerra, Antonio, Jaillon, Olivier, Wincker, Patrick, Ogata, Hiroyuki, Krupovic, Mart, Delmont, Tom O.·2021·Nature

Preprint — published as 10.1038/s41586-023-05962-4 · Paper page

Abstract

DNA viruses have a major influence on the ecology and evolution of cellular organisms, but their overall diversity and evolutionary trajectories remain elusive. Here, we performed a phylogeny-guided genome-resolved metagenomic survey of the sunlit oceans and discovered plankton-infecting relatives of herpesviruses that form a putative new phylum dubbed ‘ Mirusviricota ’. The virion morphogenesis module of this large monophyletic clade is typical of viruses from the realm Duplodnaviria , with the major capsid protein fold being a likely structural intermediate between the capsid proteins of Caudoviricetes (tailed phages) and Herpesvirales (animal-infecting viruses). Yet, a substantial fraction of ‘ Mirusviricota’ genes, including hallmark transcription machinery genes missing in herpesviruses, are closely related homologs of large and giant eukaryotic DNA viruses from another viral realm. The remarkable chimeric attributes of ‘ Mirusviricota ’ provide missing links in the evolution of both herpesviruses and giant viruses. Furthermore, mirusviruses are widespread and transcriptionally active from pole to pole, encoding complex functional traits used during the infection of microbial eukaryotes. The ‘ Mirusviricota ’ prevalence, functional activity, diversification, and atypical evolutionary traits point to a lasting role of mirusviruses in the ecology of marine ecosystems that might have not only predated but also contributed to the emergence of herpesviruses and giant viruses.

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Metadata

Authors
Gaïa, M., Meng, L., Pelletier, E., Forterre, P., Vanni, C., Fernandez-Guerra, A., Jaillon, O., Wincker, P., Ogata, H., Krupovic, M., & Delmont, T. O.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Kyoto University Institute for Chemical Research (JP)
  • University of Bremen (DE)
Corresponding author
Delmont, Tom O.
Venue
Nature
Publisher
openRxiv
Published
2021-12-27
Volume
616
Issue
7958
Pages
783-789
ISSN
0028-0836 (ISSN-L)
OpenAlex
W4366401148
Cited by
108
References
1
Citations by year
2026: 21 · 2025: 36 · 2024: 29 · 2023: 19 · 2022: 3
FWCI
16.95
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
  • Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by)
  • HAL AMU (submittedVersion)
  • HAL (submittedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
  • Kyoto University Research Information Repository (Kyoto University) (submittedVersion, cc-by)
Funders
  • Agence Nationale de la Recherche (ANR-14-CE23-0001, ANR-10-INBS-0009, ANR- 10-INBS-09, ANR-21-CE11-0001, ANR‐17‐CE02, ANR-20-CE20-0009, ANR-17-CE02-0012, ANR-17, ANR-10, 10-INBS-09)
  • Centre National de la Recherche Scientifique
  • Grand Équipement National De Calcul Intensif (t2014036389, t2016036389, t2011076389, t2015036389, t2012076389, t2013036389)
  • Japan Society for the Promotion of Science (18H02279, 22H00384)
  • Institute for Chemical Research, Kyoto University (2021-29, 2022-26, 2020-28)
  • Kyoto University Research Coordination Alliance
Topics
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Immunology and Microbiology › Virology › Plant and Fungal Interactions Research
  • Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Keywords
herpesvirus, giant viruses, viral evolution, viral metagenomics, viral ecology
MeSH terms
Giant Viruses, Animals, Herpesviridae, Oceans and Seas, Phylogeny, Plankton, Sunlight, Transcription, Genetic, Genome, Viral, Ecosystem, Metagenome, Metagenomics, Eukaryota, Aquatic Organisms

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