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, Tom O. Delmont*

*Corresponding author af dette arbejde

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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.

OriginalsprogEngelsk
TidsskriftNature
Vol/bind616
Udgave nummer7958
Sider (fra-til)783-789
Antal sider7
ISSN0028-0836
DOI
StatusUdgivet - 2023

Bibliografisk note

Funding Information:
Our survey was made possible by two scientific endeavours: the sampling and sequencing efforts by the Tara Oceans Project, and the bioinformatics and visualization capabilities afforded by anvi’o (https://anvio.org/). We are indebted to all who contributed to these efforts, as well as other open-source bioinformatics tools for their commitment to transparency and openness. Tara Oceans (which includes the Tara Oceans and Tara Oceans Polar Circle expeditions) would not exist without the leadership of the Tara Oceans Foundation and the continuous support of 23 institutes (https://oceans.taraexpeditions.org/). We also acknowledge the commitment of the CNRS and Genoscope/CEA. Some of the computations were carried out using the platine, titane and curie high-performance computing machine provided through GENCI grants (t2011076389, t2012076389, t2013036389, t2014036389, t2015036389 and t2016036389). This study was supported in part by FRANCE GENOMIQUE (ANR-10-INBS-09), the Japan Society for the Promotion of Science KAKENHI (18H02279 and 22H00384), the Research Unit for Development of Global Sustainability, Kyoto University Research Coordination Alliance, and the International Collaborative Research Program of the Institute for Chemical Research, Kyoto University (2022-26, 2021-29 and 2020-28). M.K. was supported by grants from the l’Agence Nationale de la Recherche (ANR-20-CE20-0009-02 and ANR-21-CE11-0001-01), M.G. was supported by ANR ALGALVIRUS ANR-17-CE02-0012, and T.O.D. was supported by ANR HYDROGEN ANR-14-CE23-0001. Part of the computational work was carried out at the SuperComputer System, Institute for Chemical Research, Kyoto University. This article is contribution number 141 of Tara Oceans.

Publisher Copyright:
© 2023, The Author(s).

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