Genomic adaptation of giant viruses in polar oceans.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
12 10 2023
Historique:
received: 21 02 2023
accepted: 24 09 2023
medline: 1 11 2023
pubmed: 13 10 2023
entrez: 12 10 2023
Statut: epublish

Résumé

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.

Identifiants

pubmed: 37828003
doi: 10.1038/s41467-023-41910-6
pii: 10.1038/s41467-023-41910-6
pmc: PMC10570341
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6233

Informations de copyright

© 2023. Springer Nature Limited.

Références

Nature. 2020 Dec;588(7836):141-145
pubmed: 33208937
Nat Ecol Evol. 2019 Mar;3(3):469-478
pubmed: 30804520
Proc Natl Acad Sci U S A. 2019 Oct 8;116(41):20574-20583
pubmed: 31548428
PLoS Biol. 2021 Oct 27;19(10):e3001430
pubmed: 34705818
Nature. 2016 Apr 28;532(7600):465-470
pubmed: 26863193
iScience. 2020 Dec 29;24(1):102002
pubmed: 33490910
Bioinformatics. 2018 Mar 15;34(6):1053-1055
pubmed: 29091997
Adv Virus Res. 2019;103:167-202
pubmed: 30635076
Science. 2022 Jun 10;376(6598):1202-1208
pubmed: 35679415
Cell Genom. 2022 Apr 28;2(5):100123
pubmed: 36778897
ISME J. 2013 Sep;7(9):1827-41
pubmed: 23657361
Sci Adv. 2021 Aug 27;7(35):
pubmed: 34452910
Science. 2017 Apr 7;356(6333):82-85
pubmed: 28386012
Microbes Environ. 2018 Jul 4;33(2):162-171
pubmed: 29806626
Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):10913-8
pubmed: 16043709
Virology. 2005 Oct 10;341(1):80-90
pubmed: 16081120
Viruses. 2016 Mar 01;8(3):66
pubmed: 26938550
mSphere. 2021 Apr 21;6(2):
pubmed: 33883262
BMC Genomics. 2020 Aug 6;21(1):543
pubmed: 32758141
Virology. 2014 Oct;466-467:60-70
pubmed: 25035289
Mol Biol Evol. 2021 Dec 9;38(12):5825-5829
pubmed: 34597405
Bioinformatics. 2010 Jun 1;26(11):1463-4
pubmed: 20395285
Bioinformatics. 2014 Aug 1;30(15):2216-8
pubmed: 24728855
Bioinformatics. 2014 May 1;30(9):1236-40
pubmed: 24451626
Viruses. 2021 Jan 20;13(2):
pubmed: 33498458
Science. 1988 Mar 4;239(4844):1145-7
pubmed: 2830673
Nature. 2020 Feb;578(7795):432-436
pubmed: 31968354
Mol Biol Evol. 2016 Jun;33(6):1635-8
pubmed: 26921390
Bioinformatics. 2019 Feb 1;35(3):526-528
pubmed: 30016406
Elife. 2022 Mar 31;11:
pubmed: 35356891
Cell Host Microbe. 2021 Feb 10;29(2):250-266.e8
pubmed: 33434515
Nat Methods. 2020 Mar;17(3):261-272
pubmed: 32015543
Virology. 2001 Nov 25;290(2):272-80
pubmed: 11883191
Bioinformatics. 2010 Oct 1;26(19):2460-1
pubmed: 20709691
Proc Natl Acad Sci U S A. 2010 Nov 9;107(45):19508-13
pubmed: 20974979
Nat Commun. 2018 Jan 25;9(1):373
pubmed: 29371626
Plant Cell. 2014 Jun 10;26(6):2689-2707
pubmed: 24920329
Ecol Lett. 2021 Jun;24(6):1133-1144
pubmed: 33877734
Am Nat. 2004 Feb;163(2):192-211
pubmed: 14970922
mSystems. 2021 Aug 31;6(4):e0029321
pubmed: 34254826
Nat Methods. 2021 Apr;18(4):366-368
pubmed: 33828273
Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296
pubmed: 33885785
J Virol. 2022 Apr 13;96(7):e0197021
pubmed: 35285686
J Virol. 2021 Feb 3;95(8):
pubmed: 33536167
Genome Res. 2003 Nov;13(11):2498-504
pubmed: 14597658
Front Microbiol. 2020 May 14;11:824
pubmed: 32477293
J Virol. 2012 Apr;86(8):4611-9
pubmed: 22318150
Intervirology. 2010;53(5):284-92
pubmed: 20551680
Proc Natl Acad Sci U S A. 1982 Jan;79(2):335-9
pubmed: 6952188
Proc Natl Acad Sci U S A. 2019 Sep 24;116(39):19585-19592
pubmed: 31506349
Sci Rep. 2021 Nov 24;11(1):22877
pubmed: 34819553
Proc Natl Acad Sci U S A. 2011 Apr 12;108(15):6163-8
pubmed: 21444812
Cell. 2019 May 16;177(5):1109-1123.e14
pubmed: 31031001
Mol Biol Evol. 2020 May 1;37(5):1530-1534
pubmed: 32011700
Microbiome. 2021 Feb 1;9(1):37
pubmed: 33522966
Proc Natl Acad Sci U S A. 2016 Mar 15;113(11):E1516-25
pubmed: 26929361
Front Immunol. 2021 Apr 29;12:638573
pubmed: 33995356
Genome Biol Evol. 2016 Dec 14;8(11):3351-3363
pubmed: 27811174
Genome Biol. 2008;9(7):R106
pubmed: 18598358
Cell Syst. 2019 Sep 25;9(3):286-296.e8
pubmed: 31542415
PLoS Biol. 2022 Nov 28;20(11):e3001893
pubmed: 36441816
Nature. 2023 Apr;616(7958):783-789
pubmed: 37076623
Nature. 2006 Sep 7;443(7107):43
pubmed: 16957723
BMC Bioinformatics. 2010 Mar 08;11:119
pubmed: 20211023
ISME J. 2017 Mar;11(3):601-612
pubmed: 28085157
Nat Rev Microbiol. 2007 Oct;5(10):801-12
pubmed: 17853907
Nat Ecol Evol. 2020 Dec;4(12):1639-1649
pubmed: 32895519
Nat Commun. 2020 Apr 6;11(1):1710
pubmed: 32249765
Science. 2009 Nov 6;326(5954):858-61
pubmed: 19892985
Cell. 2019 Nov 14;179(5):1084-1097.e21
pubmed: 31730851
BMC Genomics. 2019 Jul 23;20(1):605
pubmed: 31337355
ISME J. 2013 Sep;7(9):1678-95
pubmed: 23575371
Virol J. 2009 Dec 17;6:223
pubmed: 20017929
Nat Microbiol. 2022 Feb;7(2):327-336
pubmed: 34972821
PeerJ. 2015 Oct 08;3:e1319
pubmed: 26500826

Auteurs

Lingjie Meng (L)

Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan.

Tom O Delmont (TO)

Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, F-91057, Evry, France.
Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, F-75016, Paris, France.

Morgan Gaïa (M)

Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, F-91057, Evry, France.
Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, F-75016, Paris, France.

Eric Pelletier (E)

Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, F-91057, Evry, France.
Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, F-75016, Paris, France.

Antonio Fernàndez-Guerra (A)

Lundbeck Foundation GeoGenetics Centre, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.

Samuel Chaffron (S)

Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, F-75016, Paris, France.
Nantes Université, École Centrale Nantes, CNRS, LS2N, UMR 6004, F-44000, Nantes, France.

Russell Y Neches (RY)

Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan.

Junyi Wu (J)

Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan.

Hiroto Kaneko (H)

Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan.

Hisashi Endo (H)

Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan.

Hiroyuki Ogata (H)

Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan. ogata@kuicr.kyoto-u.ac.jp.

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