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Cited by 7Aquaculture disease management and microbiotaBacteriophages and microbial interactionsEvolution and Genetic Dynamics

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Viromes of Antarctic fish resemble the diversity found at lower latitudes

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Grimwood, Rebecca M, Waller, Stephanie J, Wierenga, Janelle R, Lim, Lauren, Dubrulle, Jérémy, Holmes, Edward C, Geoghegan, Jemma L·2024·Virus Evolution
DOI 10.1093/ve/veae050PMC PMC11282168

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Abstract

Antarctica harbours some of the most isolated and extreme environments on Earth, concealing a largely unexplored and unique component of the global animal virosphere. To understand the diversity and evolutionary histories of viruses in these polar species, we determined the viromes of gill metatranscriptomes from 11 Antarctic fish species with 248 samples collected from the Ross Sea region spanning the Perciformes, Gadiformes, and Scorpaeniformes orders. The continent’s shift southward and cooling temperatures >20 million years ago led to a reduction in biodiversity and subsequent radiation of some marine fauna, such as the notothenioid fishes. Despite decreased host species richness in polar regions, we revealed a surprisingly complex virome diversity in Ross Sea fish, with the types and numbers of viruses per host species and individuals sampled comparable to that of fish in warmer marine environments with higher host community diversity. We also observed a higher number of closely related viruses likely representing instances of recent and historic host-switching events among the Perciformes (all notothenioids) than in the Gadiformes, suggesting that rapid speciation events within this order generated closely related host species with few genetic barriers to cross-species transmission. Additionally, we identified novel genomic variation in an arenavirus with a split nucleoprotein sequence containing a stable helical structure, indicating potential adaptation of viral proteins to extreme temperatures. These findings enhance our understanding of virus evolution and virus-host interactions in response to environmental shifts, especially in less diverse ecosystems that are more vulnerable to the impacts of anthropogenic and climate changes.

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Research works printed but not linked: 88

  1. Aguirre de Cárcer, 2016, Metagenomic analysis of lacustrine viral diversity along a latitudinal transect of the Antarctic Peninsula, FEMS Microbiol Ecol, 92, 10.1093/femsec/fiw074 · DOI
  2. Brierley, 2006, Programmed ribosomal frameshifting in HIV-1 and the SARS–CoV, Virus Res, 119, 29, 10.1016/j.virusres.2005.10.008 · DOI
  3. Buchfink, 2021, Sensitive protein alignments at tree-of-life scale using DIAMOND, Nat Methods, 18, 366, 10.1038/s41592-021-01101-x · DOI · Paper page
  4. Burge, 2014, Climate change influences on marine infectious diseases: implications for management and society, Ann Rev Mar Sci, 6, 249, 10.1146/annurev-marine-010213-135029 · DOI
  5. Camacho, 2009, BLAST+: architecture and applications, BMC Bioinf, 10, 10.1186/1471-2105-10-421 · DOI · Paper page
  6. Capella-Gutiérrez, 2009, trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses, Bioinformatics, 25, 1972, 10.1093/bioinformatics/btp348 · DOI
  7. Charleston, 2002, Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny, Syst Biol, 51, 528, 10.1080/10635150290069940 · DOI
  8. Chen, 2013, Antigenic analysis of grass carp reovirus using single-chain variable fragment antibody against IgM from Ctenopharyngodon idella, Sci China Life Sci, 56, 59, 10.1007/s11427-012-4425-5 · DOI
  9. Clarke, 1996, Evolution and adaptive radiation of Antarctic fishes, Trends Ecol Evol, 11, 212, 10.1016/0169-5347(96)10029-X · DOI
  10. Cobo, 2016, Viruses causing hemorrhagic fever. Safety laboratory procedures, Open Virol J, 10, 1, 10.2174/1874357901610010001 · DOI
  11. Cohen, 2020, Divergent impacts of warming weather on wildlife disease risk across climates, Science, 370, 10.1126/science.abb1702 · DOI
  12. Collins, 2010, The Patagonian toothfish: biology, ecology and fishery, Adv Mar Biol, 58, 227, 10.1016/B978-0-12-381015-1.00004-6 · DOI
  13. Costa, 2023, Limited cross-species virus transmission in a spatially restricted coral reef fish community, Virus Evol, 9, 10.1093/ve/vead011 · DOI
  14. Costa, 2024, Limited transmission of microbial species among coral reef fishes from the Great Barrier Reef, Australia, Curr Biol, 34, 1247, 10.1016/j.cub.2024.02.008 · DOI
  15. Costa, 2021, Metagenomic sequencing reveals a lack of virus exchange between native and invasive freshwater fish across the Murray-Darling Basin, Australia, Virus Evol, 7, 10.1093/ve/veab034 · DOI
  16. Costa, 2023, Host adaptive radiation is associated with rapid virus diversification and cross-species transmission in African cichlid fishes, BioRxiv
  17. Cummings, 2021, Ross Sea benthic ecosystems: macro- and mega-faunal community patterns from a multi-environment survey, Front Mar Sci, 8, 10.3389/fmars.2021.629787 · DOI
  18. Daane, 2022, Adaptations and diversity of Antarctic fishes: a genomic perspective, Annu Rev Anim Biosci, 10, 39, 10.1146/annurev-animal-081221-064325 · DOI
  19. Danovaro, 2011, Marine viruses and global climate change, FEMS Microbiol Rev, 35, 993, 10.1111/j.1574-6976.2010.00258.x · DOI
  20. De’ath, 2012, The 27-year decline of coral cover on the Great Barrier Reef and its causes, Proc Natl Acad Sci, 109, 17995, 10.1073/pnas.1208909109 · DOI
  21. Devries, 1971, Glycoproteins as biological antifreeze agents in Antarctic fishes, Science, 172, 1152, 10.1126/science.172.3988.1152 · DOI
  22. Dill, 2016, Distinct viral lineages from fish and amphibians reveal the complex evolutionary history of hepadnaviruses, J Virol, 90, 7920, 10.1128/JVI.00832-16 · DOI
  23. Duffy, 2016, Biodiversity enhances reef fish biomass and resistance to climate change, Proc Natl Acad Sci, 113, 6230, 10.1073/pnas.1524465113 · DOI
  24. Eastman, 2005, The nature of the diversity of Antarctic fishes, Polar Biol, 28, 93, 10.1007/s00300-004-0667-4 · DOI
  25. Eastman, 1998, Fishes of Antarctica, 3, 10.1007/978-88-470-2157-0_1 · DOI
  26. Eastman, 1999, The fish fauna of the Ross Sea, Antarctica, Antarct Sci, 11, 293, 10.1017/S0954102099000383 · DOI
  27. Escobar, 2018, Infectious disease in fish: global risk of viral hemorrhagic septicemia virus, Rev Fish Biol Fish, 28, 637, 10.1007/s11160-018-9524-3 · DOI
  28. Eskandari, 2020, Antifreeze proteins and their practical utilization in industry, medicine, and agriculture, Biomolecules, 10, 10.3390/biom10121649 · DOI
  29. Feller, 2018, Protein folding at extreme temperatures: current issues, Semin Cell Dev Biol, 84, 129, 10.1016/j.semcdb.2017.09.003 · DOI
  30. Filipa-Silva, 2020, The unexplored virome of two Atlantic coast fish: contribution of next-generation sequencing to fish virology, Foods, 9, 10.3390/foods9111634 · DOI
  31. Ford, 2024, Five species of wild freshwater sport fish in Wisconsin, USA, reveal highly diverse viromes, Pathogens, 13, 10.3390/pathogens13020150 · DOI
  32. Geoghegan, 2021, Virome composition in marine fish revealed by meta-transcriptomics, Virus Evol, 7
  33. Gille, 2002, Warming of the Southern Ocean since the 1950s, Science, 295, 1275, 10.1126/science.1065863 · DOI
  34. Gong, 2018, Viral diversity and its relationship with environmental factors at the surface and deep sea of Prydz Bay, Antarctica, Front Microbiol, 9, 10.3389/fmicb.2018.02981 · DOI
  35. Grabherr, 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nat Biotechnol, 29, 644, 10.1038/nbt.1883 · DOI
  36. Guindon, 2010, New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0, Syst Biol, 59, 307, 10.1093/sysbio/syq010 · DOI · Paper page
  37. Hershberger, 2009, Prevalence of viral Erythrocytic necrosis in pacific herring and epizootics in Skagit Bay, Puget Sound, Washington, J Aquatic Animal Health, 21, 1, 10.1577/H08-035.1 · DOI
  38. Hoang, 2018, UFBoot2: improving the ultrafast bootstrap approximation, Mol Biol Evol, 35, 518, 10.1093/molbev/msx281 · DOI · Paper page
  39. Holm, 2022, Dali server: structural unification of protein families, Nucleic Acids Res, 50, W210, 10.1093/nar/gkac387 · DOI
  40. Jung, 2017, Rock bream iridovirus (RBIV) replication in rock bream (Oplegnathus fasciatus) exposed for different time periods to susceptible water temperatures, Fish Shellfish Immunol, 70, 731, 10.1016/j.fsi.2017.09.038 · DOI
  41. Katoh, 2013, MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol Biol Evol, 30, 772, 10.1093/molbev/mst010 · DOI · Paper page
  42. Kim, 1999, Encyclopedia of Virology, 558, 10.1006/rwvi.1999.0100 · DOI
  43. Kordas, 2011, Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems, J Exp Mar Biol Ecol, 400, 218, 10.1016/j.jembe.2011.02.029 · DOI
  44. Kraberger, 2022, Discovery of novel fish papillomaviruses: from the Antarctic to the commercial fish market, Virology, 565, 65, 10.1016/j.virol.2021.10.007 · DOI
  45. Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat Methods, 9, 357, 10.1038/nmeth.1923 · DOI · Paper page
  46. Lauber, 2017, Deciphering the origin and evolution of hepatitis B viruses by means of a family of non-enveloped fish viruses, Cell Host Microbe, 22, 387, 10.1016/j.chom.2017.07.019 · DOI
  47. Lefkowitz, 2018, Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV), Nucleic Acids Res, 46, D708, 10.1093/nar/gkx932 · DOI
  48. Li, 2011, RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome, BMC Bioinf, 12, 10.1186/1471-2105-12-323 · DOI · Paper page
  49. Li, 2015, MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph, Bioinformatics, 31, 1674, 10.1093/bioinformatics/btv033 · DOI
  50. Li, 2023, The evolutionary history of hepaciviruses, BioRxiv
  51. Littlepage, 2013, Oceanographic investigations in McMurdo Sound, Antarctica, Antarct Res Ser, 2, 1
  52. Longdon, 2014, The evolution and genetics of virus host shifts, PLoS Pathog, 10, 10.1371/journal.ppat.1004395 · DOI
  53. Lopez, 2023, Diverse microvirus genomes identified in the stomach of a sharp-spined Notothen (Trematomus pennellii) from the Ross Sea (East Antarctica), Microbiol Resour Announc, 12, e01233, 10.1128/mra.01233-22 · DOI
  54. Marsh, 2010, How do proteins gain new domains?, Genome Biol, 11, 10.1186/gb-2010-11-7-126 · DOI
  55. Miller, 2021, Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae, Virus Evol, 7, 10.1093/ve/veab050 · DOI
  56. Mirdita, 2022, ColabFold: making protein folding accessible to all, Nat Methods, 19, 679, 10.1038/s41592-022-01488-1 · DOI · Paper page
  57. Mordecai, 2019, Endangered wild salmon infected by newly discovered viruses, eLife, 8, 10.7554/eLife.47615 · DOI
  58. Nelson, 2006, Fishes of the World
  59. Nguyen, 2015, IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol Biol Evol, 32, 268, 10.1093/molbev/msu300 · DOI · Paper page
  60. Nye, 2009, Changing spatial distribution of fish stocks in relation to climate and population size on the Northeast United States continental shelf, Mar Ecol Prog Ser, 393, 111, 10.3354/meps08220 · DOI · Paper page
  61. Nylund, 2008, Morphogenesis of salmonid gill poxvirus associated with proliferative gill disease in farmed Atlantic salmon (Salmo salar) in Norway, Arch Virol, 153, 1299, 10.1007/s00705-008-0117-7 · DOI
  62. Oksanen, 2022, vegan: Community Ecology Package
  63. Páez, 2021, Temperature variation and host immunity regulate viral persistence in a salmonid host, Pathogens, 10, 10.3390/pathogens10070855 · DOI
  64. Papageorgiou, 2021, Observation of arenavirus nucleoprotein heptamer assembly, FEBS Open Bio, 11, 1076, 10.1002/2211-5463.13106 · DOI
  65. Parry, 2020, Divergent influenza-like viruses of amphibians and fish support an ancient evolutionary association, Viruses, 12, 10.3390/v12091042 · DOI
  66. Peck, 2018, Complexities of viral mutation rates, J Virol, 92, 10, 10.1128/JVI.01031-17 · DOI
  67. Perry, 2022, Viromes of freshwater fish with lacustrine and diadromous life histories differ in composition, Viruses, 14, 10.3390/v14020257 · DOI
  68. Pettersen, 2021, UCSF ChimeraX: structure visualization for researchers, educators, and developers, Protein Sci, 30, 70, 10.1002/pro.3943 · DOI
  69. Pontremoli, 2019, Arenavirus genomics: novel insights into viral diversity, origin, and evolution, Curr Opin Virol, 34, 18, 10.1016/j.coviro.2018.11.001 · DOI
  70. Rabosky, 2018, An inverse latitudinal gradient in speciation rate for marine fishes, Nature, 559, 392, 10.1038/s41586-018-0273-1 · DOI
  71. Reuter, 2022, A novel parvovirus (family Parvoviridae) in a freshwater fish, zander (Sander lucioperca), Arch Virol, 167, 1163, 10.1007/s00705-022-05419-5 · DOI
  72. Robichaux, 2016, Validation of RPS13 as a reference gene for absolute quantification of SIV RNA in tissue of rhesus macaques, J Virol Methods, 236, 245, 10.1016/j.jviromet.2016.08.004 · DOI
  73. Sandlund, 2021, Comparative molecular characterization of novel and known piscine toti-like viruses, Viruses, 13, 10.3390/v13061063 · DOI
  74. Seehausen, 2006, African cichlid fish: a model system in adaptive radiation research, Proc R Soc B, 273, 1987, 10.1098/rspb.2006.3539 · DOI
  75. Shi, 2018, The evolutionary history of vertebrate RNA viruses, Nature, 556, 197, 10.1038/s41586-018-0012-7 · DOI
  76. Smeele, 2018, Viruses associated with Antarctic wildlife: from serology based detection to identification of genomes using high throughput sequencing, Virus Res, 243, 91, 10.1016/j.virusres.2017.10.017 · DOI
  77. Smith, 2012, Antarctic Ecosystems, 213, 10.1002/9781444347241.ch7 · DOI
  78. Snel, 2000, Genome evolution, Trends Genet, 16, 9, 10.1016/S0168-9525(99)01924-1 · DOI
  79. Tartor, 2022, Emergence of Salmon gill poxvirus, Viruses, 14, 10.3390/v14122701 · DOI
  80. Thacker, 2021, Delayed adaptive radiation among New Zealand stream fishes: joint estimation of divergence time and trait evolution in a newly delineated island species flock, Syst Biol, 71, 13, 10.1093/sysbio/syab014 · DOI
  81. Van Doorslaer, 2018, Fish polyomaviruses belong to two distinct evolutionary lineages, J Gen Virol, 99, 567, 10.1099/jgv.0.001041 · DOI
  82. Varsani, 2017, Identification of a polyomavirus in Weddell seal (Leptonychotes weddellii) from the Ross Sea (Antarctica), Arch Virol, 162, 1403, 10.1007/s00705-017-3239-y · DOI
  83. Watashi, 2015, Hepatitis B virus and hepatitis D virus entry, species specificity, and tissue tropism, Cold Spring Harb Perspect Med, 5, 10.1101/cshperspect.a021378 · DOI
  84. Wickham, 2016, Ggplot2: Elegant Graphics for Data Analysis, 10.1007/978-3-319-24277-4 · DOI
  85. Wille, 2020, Sustained RNA virome diversity in Antarctic penguins and their ticks, ISME J, 14, 1768, 10.1038/s41396-020-0643-1 · DOI
  86. Wille, 2020, Wild birds as reservoirs for diverse and abundant gamma- and deltacoronaviruses, FEMS Microbiol Rev, 44, 631, 10.1093/femsre/fuaa026 · DOI
  87. Xi, 2023, Viromics reveals the high diversity of viruses from fishes of the Tibet highland, Microbiol Spectr, 11, e00946, 10.1128/spectrum.00946-23 · DOI
  88. Zhang, 2007, Isolation and characterization of Scophthalmus maximus rhabdovirus, Dis Aquat Organ, 74, 95, 10.3354/dao074095 · DOI

Metadata

Authors
Grimwood, R. M., Waller, S. J., Wierenga, J. R., Lim, L., Dubrulle, J., Holmes, E. C., & Geoghegan, J. L.
Affiliations
  • University of Otago (NZ)
  • The University of Sydney (AU)
  • Department of Microbiology and Immunology, University of Otago , Dunedin 9016, New Zealand
  • New Zealand Institute for Public Health and Forensic Science (NZ)
Corresponding author
Geoghegan, Jemma L
ORCID
Venue
Virus Evolution
Publisher
Oxford University Press (OUP)
Published
2024
Volume
10
Issue
1
Pages
veae050-veae050
ISSN
2057-1577 (ISSN-L)
DOI
10.1093/ve/veae050
PMC
PMC11282168
OpenAlex
W4400640192
Cited by
7
References
2
Citations by year
2026: 5 · 2025: 2
FWCI
1.16
Type
journal article
Language
en
Open access
Licence
Locations
  • Virus Evolution (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Health and Medical Research Council (GNT2017197)
  • New Zealand Ministry of Business, Innovation and Employment, Endeavour programme (CAWX2207)
  • New Zealand Royal Society Rutherford Discovery Fellowship (RDF-20-UOO-007)
  • Marsden Fund (20-UOO-105)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
fish viruses, notothenioid fishes, host switching, viral evolution, arenaviruses, thermal adaptation, Ross Sea, viral diversity, host-virus interaction, climate change vulnerability

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