1887

Abstract

is a diverse family of circular, double-stranded DNA (dsDNA) viruses that infect a broad range of mammalian, avian and fish hosts. While papillomaviruses have been characterized most extensively in humans, the study of non-human papillomaviruses has contributed greatly to our understanding of their pathogenicity and evolution. Using high-throughput sequencing approaches, we identified 7 novel papillomaviruses from vaginal swabs collected from 81 adult female Weddell seals () in the Ross Sea of Antarctica between 2014–2017. These seven papillomavirus genomes were amplified from seven individual seals, and six of the seven genomes represented novel species with distinct evolutionary lineages. This highlights the diversity of papillomaviruses among the relatively small number of Weddell seal samples tested. Viruses associated with large vertebrates are poorly studied in Antarctica, and this study adds information about papillomaviruses associated with Weddell seals and contributes to our understanding of the evolutionary history of papillomaviruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001028
2018-04-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/4/549.html?itemId=/content/journal/jgv/10.1099/jgv.0.001028&mimeType=html&fmt=ahah

References

  1. Rector A, van Ranst M. Animal papillomaviruses. Virology 2013; 445:213–223 [View Article][PubMed]
    [Google Scholar]
  2. Doorbar J. The papillomavirus life cycle. J Clin Virol 2005; 32:7–15 [View Article]
    [Google Scholar]
  3. Münger K, Scheffner M, Huibregtse JM, Howley PM. Interactions of HPV E6 and E7 oncoproteins with tumour suppressor gene products. Cancer Surv 1992; 12:197–217[PubMed]
    [Google Scholar]
  4. Münger K, Werness BA, Dyson N, Phelps WC, Harlow E et al. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J 1989; 8:4099–4105[PubMed]
    [Google Scholar]
  5. Yew PR, Berk AJ. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature 1992; 357:82–85 [View Article][PubMed]
    [Google Scholar]
  6. Dyson N, Howley PM, Münger K, Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 1989; 243:934–937 [View Article][PubMed]
    [Google Scholar]
  7. López-Bueno A, Mavian C, Labella AM, Castro D, Borrego JJ et al. Concurrence of iridovirus, polyomavirus, and a unique member of a new group of fish papillomaviruses in lymphocystis disease-affected gilthead sea bream. J Virol 2016; 90:8768–8779 [View Article][PubMed]
    [Google Scholar]
  8. van Doorslaer K, Ruoppolo V, Schmidt A, Lescroël A, Jongsomjit D et al. Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins. Virus Evol 2017; 3:vex027 [View Article][PubMed]
    [Google Scholar]
  9. Smeele ZE, Ainley DG, Varsani A. Viruses associated with Antarctic wildlife: From serology based detection to identification of genomes using high throughput sequencing. Virus Res 2018; 243:91–105 [View Article][PubMed]
    [Google Scholar]
  10. Lee SY, Kim JH, Park YM, Shin OS, Kim H et al. A novel adenovirus in Chinstrap penguins (Pygoscelis antarctica) in Antarctica. Viruses 2014; 6:2052–2061 [View Article][PubMed]
    [Google Scholar]
  11. Lee SY, Kim JH, Seo TK, No JS, Kim H et al. Genetic and molecular epidemiological characterization of a novel adenovirus in Antarctic penguins collected between 2008 and 2013. PLoS One 2016; 11:e0157032 [View Article][PubMed]
    [Google Scholar]
  12. Park YM, Kim JH, Gu SH, Lee SY, Lee MG et al. Full genome analysis of a novel adenovirus from the South Polar skua (Catharacta maccormicki) in Antarctica. Virology 2012; 422:144–150 [View Article][PubMed]
    [Google Scholar]
  13. Fahsbender E, Burns JM, Kim S, Kraberger S, Frankfurter G et al. Diverse and highly recombinant anelloviruses associated with Weddell seals in Antarctica. Virus Evol 2017; 3:vex017 [View Article][PubMed]
    [Google Scholar]
  14. Hurt AC, Su YC, Aban M, Peck H, Lau H et al. Evidence for the introduction, reassortment, and persistence of diverse influenza a viruses in Antarctica. J Virol 2016; 90:9674–9682 [View Article][PubMed]
    [Google Scholar]
  15. Hurt AC, Vijaykrishna D, Butler J, Baas C, Maurer-Stroh S et al. Detection of evolutionarily distinct avian influenza a viruses in Antarctica. MBio 2014; 5:e01098-14 [View Article][PubMed]
    [Google Scholar]
  16. Varsani A, Kraberger S, Jennings S, Porzig EL, Julian L et al. A novel papillomavirus in Adélie penguin (Pygoscelis adeliae) faeces sampled at the Cape Crozier colony, Antarctica. J Gen Virol 2014; 95:1352–1365 [View Article][PubMed]
    [Google Scholar]
  17. Goraichuk IV, Dimitrov KM, Sharma P, Miller PJ, Swayne DE et al. Complete genome sequences of four avian paramyxoviruses of serotype 10 isolated from Rockhopper Penguins on the Falkland Islands. Genome Announc 2017; 5:e00472-17 [View Article][PubMed]
    [Google Scholar]
  18. Miller PJ, Afonso CL, Spackman E, Scott MA, Pedersen JC et al. Evidence for a new avian paramyxovirus serotype 10 detected in rockhopper penguins from the Falkland Islands. J Virol 2010; 84:11496–11504 [View Article][PubMed]
    [Google Scholar]
  19. Neira V, Tapia R, Verdugo C, Barriga G, Mor S et al. Novel avulaviruses in penguins, Antarctica. Emerg Infect Dis 2017; 23:1212–1214 [View Article][PubMed]
    [Google Scholar]
  20. Thomazelli LM, Araujo J, Oliveira DB, Sanfilippo L, Ferreira CS et al. Newcastle disease virus in penguins from King George Island on the Antarctic region. Vet Microbiol 2010; 146:155–160 [View Article][PubMed]
    [Google Scholar]
  21. Buck CB, van Doorslaer K, Peretti A, Geoghegan EM, Tisza MJ et al. The ancient evolutionary history of polyomaviruses. PLoS Pathog 2016; 12:e1005574 [View Article][PubMed]
    [Google Scholar]
  22. Varsani A, Frankfurter G, Stainton D, Male MF, Kraberger S et al. Identification of a polyomavirus in Weddell seal (Leptonychotes weddellii) from the Ross Sea (Antarctica). Arch Virol 2017; 162:1403–1407 [View Article][PubMed]
    [Google Scholar]
  23. Varsani A, Porzig EL, Jennings S, Kraberger S, Farkas K et al. Identification of an avian polyomavirus associated with Adélie penguins (Pygoscelis adeliae). J Gen Virol 2015; 96:851–857 [View Article][PubMed]
    [Google Scholar]
  24. Tryland M, Klein J, Nordøy ES, Blix AS. Isolation and partial characterization of a parapoxvirus isolated from a skin lesion of a Weddell seal. Virus Res 2005; 108:83–87 [View Article][PubMed]
    [Google Scholar]
  25. Forrester NL, Palacios G, Tesh RB, Savji N, Guzman H et al. Genome-scale phylogeny of the alphavirus genus suggests a marine origin. J Virol 2012; 86:2729–2738 [View Article][PubMed]
    [Google Scholar]
  26. La Linn M, Gardner J, Warrilow D, Darnell GA, McMahon CR et al. Arbovirus of marine mammals: a new alphavirus isolated from the elephant seal louse, Lepidophthirus macrorhini. J Virol 2001; 75:4103–4109 [View Article][PubMed]
    [Google Scholar]
  27. Bininda-Emonds OR, Gittleman JL, Purvis A. Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol Rev Camb Philos Soc 1999; 74:143–175 [View Article][PubMed]
    [Google Scholar]
  28. Higdon JW, Bininda-Emonds OR, Beck RM, Ferguson SH. Phylogeny and divergence of the pinnipeds (Carnivora: Mammalia) assessed using a multigene dataset. BMC Evol Biol 2007; 7:216 [View Article][PubMed]
    [Google Scholar]
  29. Burns JM, Trumble SJ, Castellini MA, Testa JW. The diet of Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis. Polar Biol 1998; 19:272–282 [View Article]
    [Google Scholar]
  30. Stirling I. Ecology of the Weddell Seal in McMurdo Sound, Antarctica. Ecology 1969; 50:573–586 [View Article]
    [Google Scholar]
  31. Castellini MA, Davis RW, Kooyman GL. Annual Cycles of Diving Behavior and Ecology of the Weddell Seal Univ of California Press; 1991
    [Google Scholar]
  32. Rivera R, Robles-Sikisaka R, Hoffman EM, Stacy BA, Jensen ED et al. Characterization of a novel papillomavirus species (ZcPV1) from two California sea lions (Zalophus californianus). Vet Microbiol 2012; 155:257–266 [View Article][PubMed]
    [Google Scholar]
  33. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
    [Google Scholar]
  34. Wang J, Zhou D, Prabhu A, Schlegel R, Yuan H. The canine papillomavirus and gamma HPV E7 proteins use an alternative domain to bind and destabilize the retinoblastoma protein. PLoS Pathog 2010; 6:e1001089 [View Article][PubMed]
    [Google Scholar]
  35. de Villiers EM, Fauquet C, Broker TR, Bernard HU, Zur Hausen H. Classification of papillomaviruses. Virology 2004; 324:17–27 [View Article][PubMed]
    [Google Scholar]
  36. Gottschling M, Stamatakis A, Nindl I, Stockfleth E, Alonso A et al. Multiple evolutionary mechanisms drive papillomavirus diversification. Mol Biol Evol 2007; 24:1242–1258 [View Article][PubMed]
    [Google Scholar]
  37. Roman A, Munger K. The papillomavirus E7 proteins. Virology 2013; 445:138–168 [View Article][PubMed]
    [Google Scholar]
  38. Stevens H, Rector A, Bertelsen MF, Leifsson PS, van Ranst M. Novel papillomavirus isolated from the oral mucosa of a polar bear does not cluster with other papillomaviruses of carnivores. Vet Microbiol 2008; 129:108–116 [View Article][PubMed]
    [Google Scholar]
  39. Stevens H, Rector A, van der Kroght K, van Ranst M. Isolation and cloning of two variant papillomaviruses from domestic pigs: Sus scrofa papillomaviruses type 1 variants a and b. J Gen Virol 2008; 89:2475–2481 [View Article][PubMed]
    [Google Scholar]
  40. Wu Z, Ren X, Yang L, Hu Y, Yang J et al. Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces. J Virol 2012; 86:10999–11012 [View Article][PubMed]
    [Google Scholar]
  41. Zhang W, Yang S, Shan T, Hou R, Liu Z et al. Virome comparisons in wild-diseased and healthy captive giant pandas. Microbiome 2017; 5:90 [View Article][PubMed]
    [Google Scholar]
  42. van Doorslaer K. Evolution of the papillomaviridae. Virology 2013; 445:11–20 [View Article][PubMed]
    [Google Scholar]
  43. Rector A, Stevens H, Lacave G, Lemey P, Mostmans S et al. Genomic characterization of novel dolphin papillomaviruses provides indications for recombination within the Papillomaviridae. Virology 2008; 378:151–161 [View Article][PubMed]
    [Google Scholar]
  44. Rehtanz M, Ghim SJ, Rector A, van Ranst M, Fair PA et al. Isolation and characterization of the first American bottlenose dolphin papillomavirus: Tursiops truncatus papillomavirus type 2. J Gen Virol 2006; 87:3559–3565 [View Article][PubMed]
    [Google Scholar]
  45. Robles-Sikisaka R, Rivera R, Nollens HH, St Leger J, Durden WN et al. Evidence of recombination and positive selection in cetacean papillomaviruses. Virology 2012; 427:189–197 [View Article][PubMed]
    [Google Scholar]
  46. Gottschling M, Bravo IG, Schulz E, Bracho MA, Deaville R et al. Modular organizations of novel cetacean papillomaviruses. Mol Phylogenet Evol 2011; 59:34–42 [View Article][PubMed]
    [Google Scholar]
  47. van Doorslaer K, McBride AA. Molecular archeological evidence in support of the repeated loss of a papillomavirus gene. Sci Rep 2016; 6:33028 [View Article][PubMed]
    [Google Scholar]
  48. García-Vallvé S, Alonso A, Bravo IG. Papillomaviruses: different genes have different histories. Trends Microbiol 2005; 13:514–521 [View Article][PubMed]
    [Google Scholar]
  49. Varsani A, van der Walt E, Heath L, Rybicki EP, Williamson AL et al. Evidence of ancient papillomavirus recombination. J Gen Virol 2006; 87:2527–2531 [View Article][PubMed]
    [Google Scholar]
  50. Burk RD, Harari A, Chen Z. Human papillomavirus genome variants. Virology 2013; 445:232–243 [View Article][PubMed]
    [Google Scholar]
  51. McKenna MC, Bell SK. Classification of Mammals: Above the Species Level Columbia University Press; 1997
    [Google Scholar]
  52. Mengual-Chuliá B, Wittstatt U, Bravo IG. The first papillomavirus isolated from Vulpes vulpes (VvulPV1) is basal to the Gammapapillomavirus genus. Genome Announc 2015; 3:e00111-15 [View Article][PubMed]
    [Google Scholar]
  53. Ng TF, Wheeler E, Greig D, Waltzek TB, Gulland F et al. Metagenomic identification of a novel anellovirus in Pacific harbor seal (Phoca vitulina richardsii) lung samples and its detection in samples from multiple years. J Gen Virol 2011; 92:1318–1323 [View Article][PubMed]
    [Google Scholar]
  54. Smits SL, Raj VS, Oduber MD, Schapendonk CM, Bodewes R et al. Metagenomic analysis of the ferret fecal viral flora. PLoS One 2013; 8:e71595 [View Article][PubMed]
    [Google Scholar]
  55. Bravo IG, Alonso A. Phylogeny and evolution of papillomaviruses based on the E1 and E2 proteins. Virus Genes 2007; 34:249–262 [View Article][PubMed]
    [Google Scholar]
  56. Warren CJ, van Doorslaer K, Pandey A, Espinosa JM, Pyeon D. Role of the host restriction factor APOBEC3 on papillomavirus evolution. Virus Evol 2015; 1:vev015 [View Article][PubMed]
    [Google Scholar]
  57. van Doorslaer K, Desalle R, Einstein MH, Burk RD. Degradation of human PDZ-proteins by human alphapapillomaviruses represents an evolutionary adaptation to a novel cellular niche. PLoS Pathog 2015; 11:e1004980 [View Article][PubMed]
    [Google Scholar]
  58. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ et al. ABySS: a parallel assembler for short read sequence data. Genome Res 2009; 19:1117–1123 [View Article][PubMed]
    [Google Scholar]
  59. van Doorslaer K, Li Z, Xirasagar S, Maes P, Kaminsky D et al. The Papillomavirus Episteme: a major update to the papillomavirus sequence database. Nucleic Acids Res 2017; 45:D499–D506 [View Article][PubMed]
    [Google Scholar]
  60. van Doorslaer K, Tan Q, Xirasagar S, Bandaru S, Gopalan V et al. The Papillomavirus Episteme: a central resource for papillomavirus sequence data and analysis. Nucleic Acids Res 2013; 41:D571–D578 [View Article][PubMed]
    [Google Scholar]
  61. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article][PubMed]
    [Google Scholar]
  62. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article][PubMed]
    [Google Scholar]
  63. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9:772 [View Article][PubMed]
    [Google Scholar]
  64. Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 2017; 34:772–773 [View Article][PubMed]
    [Google Scholar]
  65. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 2006; 55:539–552 [View Article][PubMed]
    [Google Scholar]
  66. Stöver BC, Müller KF. TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 2010; 11:7 [View Article][PubMed]
    [Google Scholar]
  67. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article][PubMed]
    [Google Scholar]
  68. Muhire BM, Varsani A, Martin DP. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 2014; 9:e108277 [View Article][PubMed]
    [Google Scholar]
  69. Kumar S, Stecher G, Suleski M, Hedges SB. TimeTree: a resource for timelines, timetrees, and divergence times. Mol Biol Evol 2017; 34:1812–1819 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001028
Loading
/content/journal/jgv/10.1099/jgv.0.001028
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error