Genomic adaptation of giant viruses in polar oceans

Lingjie Meng, Tom O. Delmont, Morgan Gaïa, Eric Pelletier, Antonio Fernàndez-Guerra, Samuel Chaffron, Russell Y. Neches, Junyi Wu, Hiroto Kaneko, Hisashi Endo, Hiroyuki Ogata*

*Corresponding author af dette arbejde

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Abstract

Despite being perennially frigid, polar oceans form an ecosystem hosting high and unique biodiversity. Various organisms show different adaptive strategies in this habitat, but how viruses adapt to this environment is largely unknown. Viruses of phyla Nucleocytoviricota and Mirusviricota are groups of eukaryote-infecting large and giant DNA viruses with genomes encoding a variety of functions. Here, by leveraging the Global Ocean Eukaryotic Viral database, we investigate the biogeography and functional repertoire of these viruses at a global scale. We first confirm the existence of an ecological barrier that clearly separates polar and nonpolar viral communities, and then demonstrate that temperature drives dramatic changes in the virus–host network at the polar–nonpolar boundary. Ancestral niche reconstruction suggests that adaptation of these viruses to polar conditions has occurred repeatedly over the course of evolution, with polar-adapted viruses in the modern ocean being scattered across their phylogeny. Numerous viral genes are specifically associated with polar adaptation, although most of their homologues are not identified as polar-adaptive genes in eukaryotes. These results suggest that giant viruses adapt to cold environments by changing their functional repertoire, and this viral evolutionary strategy is distinct from the polar adaptation strategy of their hosts.

OriginalsprogEngelsk
Artikelnummer6233
TidsskriftNature Communications
Vol/bind14
Antal sider12
ISSN2041-1723
DOI
StatusUdgivet - 2023

Bibliografisk note

Funding Information:
This work was supported by JSPS/KAKENHI (18H02279 and 22H00384, to H.O.), and the Collaborative International Joint Research Program of the Institute for Chemical Research, Kyoto University (No. 2021-29, 2022-26 to T.O.D.; No. 2022-27, to S.C.), and the H2020 European Commission project AtlantECO (award number 862923, to S.C.). Computational time was provided by the SuperComputer System, Institute for Chemical Research, Kyoto University. We further thank the Tara Oceans consortium, and the people and sponsors who supported Tara Oceans. Tara Oceans (including both the Tara Oceans and Tara Oceans Polar Circle expeditions) would not exist without the leadership of the Tara Expeditions Foundation and the continuous support of 23 institutes (https://oceans.taraexpeditions.org). This article is contribution number 147 of Tara Oceans. We thank Gabe Yedid, PhD, from Edanz (http://jp.edanz.com) for editing a draft of this manuscript.

Funding Information:
This work was supported by JSPS/KAKENHI (18H02279 and 22H00384, to H.O.), and the Collaborative International Joint Research Program of the Institute for Chemical Research, Kyoto University (No. 2021-29, 2022-26 to T.O.D.; No. 2022-27, to S.C.), and the H2020 European Commission project AtlantECO (award number 862923, to S.C.). Computational time was provided by the SuperComputer System, Institute for Chemical Research, Kyoto University. We further thank the Tara Oceans consortium, and the people and sponsors who supported Tara Oceans. Tara Oceans (including both the Tara Oceans and Tara Oceans Polar Circle expeditions) would not exist without the leadership of the Tara Expeditions Foundation and the continuous support of 23 institutes ( https://oceans.taraexpeditions.org ). This article is contribution number 147 of Tara Oceans. We thank Gabe Yedid, PhD, from Edanz ( http://jp.edanz.com ) for editing a draft of this manuscript.

Publisher Copyright:
© 2023, Springer Nature Limited.

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