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Genomic adaptation of giant viruses in polar oceans

Author

Listed:
  • Lingjie Meng

    (Kyoto University, Gokasho)

  • Tom O. Delmont

    (Univ Evry, Université Paris-Saclay
    FR2022/Tara GOsee)

  • Morgan Gaïa

    (Univ Evry, Université Paris-Saclay
    FR2022/Tara GOsee)

  • Eric Pelletier

    (Univ Evry, Université Paris-Saclay
    FR2022/Tara GOsee)

  • Antonio Fernàndez-Guerra

    (University of Copenhagen)

  • Samuel Chaffron

    (FR2022/Tara GOsee
    École Centrale Nantes, CNRS, LS2N, UMR 6004)

  • Russell Y. Neches

    (Kyoto University, Gokasho)

  • Junyi Wu

    (Kyoto University, Gokasho)

  • Hiroto Kaneko

    (Kyoto University, Gokasho)

  • Hisashi Endo

    (Kyoto University, Gokasho)

  • Hiroyuki Ogata

    (Kyoto University, Gokasho)

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.

Suggested Citation

  • 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, 2023. "Genomic adaptation of giant viruses in polar oceans," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41910-6
    DOI: 10.1038/s41467-023-41910-6
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    References listed on IDEAS

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    1. Michiyo Yamamoto-Kawai & Eddy Carmack & Fiona McLaughlin, 2006. "Nitrogen balance and Arctic throughflow," Nature, Nature, vol. 443(7107), pages 43-43, September.
    2. Mohammad Moniruzzaman & Alaina R. Weinheimer & Carolina A. Martinez-Gutierrez & Frank O. Aylward, 2020. "Widespread endogenization of giant viruses shapes genomes of green algae," Nature, Nature, vol. 588(7836), pages 141-145, December.
    3. Mohammad Moniruzzaman & Carolina A. Martinez-Gutierrez & Alaina R. Weinheimer & Frank O. Aylward, 2020. "Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    4. Lionel Guidi & Samuel Chaffron & Lucie Bittner & Damien Eveillard & Abdelhalim Larhlimi & Simon Roux & Youssef Darzi & Stephane Audic & Léo Berline & Jennifer R. Brum & Luis Pedro Coelho & Julio Cesar, 2016. "Plankton networks driving carbon export in the oligotrophic ocean," Nature, Nature, vol. 532(7600), pages 465-470, April.
    5. Quentin Carradec & Eric Pelletier & Corinne Da Silva & Adriana Alberti & Yoann Seeleuthner & Romain Blanc-Mathieu & Gipsi Lima-Mendez & Fabio Rocha & Leila Tirichine & Karine Labadie & Amos Kirilovsky, 2018. "A global ocean atlas of eukaryotic genes," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    6. Frederik Schulz & Simon Roux & David Paez-Espino & Sean Jungbluth & David A. Walsh & Vincent J. Denef & Katherine D. McMahon & Konstantinos T. Konstantinidis & Emiley A. Eloe-Fadrosh & Nikos C. Kyrpid, 2020. "Giant virus diversity and host interactions through global metagenomics," Nature, Nature, vol. 578(7795), pages 432-436, February.
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