Mirusviruses link herpesviruses to giant viruses

Morgan Gaïa, Lingjie Meng, Eric Pelletier, Patrick Forterre, Chiara Vanni, Antonio Fernandez-Guerra, Olivier Jaillon, Patrick Wincker, Hiroyuki Ogata, Mart Krupovic and Tom O. Delmont ()
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Morgan Gaïa: Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ. Evry, Université Paris-Saclay
Lingjie Meng: Kyoto University
Eric Pelletier: Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ. Evry, Université Paris-Saclay
Patrick Forterre: Institut de Biologie Intégrative de la Cellule (I2BC), CNRS, Université Paris-Saclay
Chiara Vanni: University of Bremen
Antonio Fernandez-Guerra: University of Copenhagen
Olivier Jaillon: Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ. Evry, Université Paris-Saclay
Patrick Wincker: Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ. Evry, Université Paris-Saclay
Hiroyuki Ogata: Kyoto University
Mart Krupovic: Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit
Tom O. Delmont: Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ. Evry, Université Paris-Saclay

Nature, 2023, vol. 616, issue 7958, 783-789

Abstract: Abstract DNA viruses have a major influence on the ecology and evolution of cellular organisms1–4, but their overall diversity and evolutionary trajectories remain elusive5. Here we carried out 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 Duplodnaviria6, with multiple components strongly indicating a common ancestry with animal-infecting Herpesvirales. Yet, a substantial fraction of mirusvirus genes, including hallmark transcription machinery genes missing in herpesviruses, are closely related homologues of giant eukaryotic DNA viruses from another viral realm, Varidnaviria. These remarkable chimaeric attributes connecting Mirusviricota to herpesviruses and giant eukaryotic viruses are supported by more than 100 environmental mirusvirus genomes, including a near-complete contiguous genome of 432 kilobases. Moreover, mirusviruses are among the most abundant and active eukaryotic viruses characterized in the sunlit oceans, encoding a diverse array of functions used during the infection of microbial eukaryotes from pole to pole. The prevalence, functional activity, diversification and atypical chimaeric attributes of mirusviruses point to a lasting role of Mirusviricota in the ecology of marine ecosystems and in the evolution of eukaryotic DNA viruses.

Date: 2023
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DOI: 10.1038/s41586-023-05962-4

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