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Genomic adaptation of giant viruses in polar oceans

Meng, Lingjie Delmont, Tom O. Gaïa, Morgan Pelletier, Eric Fernàndez-Guerra, Antonio Chaffron, Samuel Neches, Russell Y. Wu, Junyi Kaneko, Hiroto Endo, Hisashi Ogata, Hiroyuki 京都大学 DOI:10.1038/s41467-023-41910-6

2023.10.12

概要

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.

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参考文献

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Acknowledgements

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, 202226 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.

Author contributions

L.M. and H.O. designed the study. L.M. performed the primary biogeographical analysis. T.O.D completed the genome-resolved metagenomic analysis. M.G. performed phylogenomic analyses. E.P. generated

the reads mapping data. A.F.-G. provided de novo clusters of viral genes.

S.C., R.Y.N., J.W., H.K., H.E. contributed to the bioinformatics analysis. All

the authors contributed to interpreting the data and writing the

manuscript.

Competing interests

The authors declare no competing interests.

Additional information

Supplementary information The online version contains

supplementary material available at

https://doi.org/10.1038/s41467-023-41910-6.

Correspondence and requests for materials should be addressed to

Hiroyuki Ogata.

Peer review information Nature Communications thanks Frank Aylward,

Chuan Ku and the other, anonymous, reviewer(s) for their contribution to

the peer review of this work. A peer review file is available.

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