1887

Abstract

Papillomaviruses are epitheliotropic viruses that have circular dsDNA genomes encapsidated in non-enveloped virions. They have been found to infect a variety of mammals, reptiles and birds, but so far they have not been found in amphibians. Using a next-generation sequencing assembly contig-informed recovery, we cloned and Sanger sequenced the complete genome of a novel papillomavirus from the faecal matter of Adélie penguins () nesting on Ross Island, Antarctica. The genome had all the usual features of a papillomavirus and an E9 ORF encoding a protein of unknown function that is found in all avian papillomaviruses to date. This novel papillomavirus genome shared ~60 % pairwise identity with the genomes of the other three known avian papillomaviruses: 1 (FcPV1), 1 (FlPV1) and 1. Pairwise identity analysis and phylogenetic analysis of the major capsid protein gene clearly indicated that it represents a novel species, which we named 1 (PaCV1). No evidence of recombination was detected in the genome of PaCV1, but we did detect a recombinant region (119 nt) in the E6 gene of FlPV1 with the recombinant region being derived from ancestral FcPV1-like sequences. Previously only paramyxoviruses, orthomyxoviruses and avian pox viruses have been genetically identified in penguins; however, the majority of penguin viral identifications have been based on serology or histology. This is the first report, to our knowledge, of a papillomavirus associated with a penguin species.

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2014-06-01
2019-10-18
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References

  1. Abascal F. , Zardoya R. , Posada D. . ( 2005; ). ProtTest: selection of best-fit models of protein evolution. . Bioinformatics 21:, 2104–2105. [CrossRef] [PubMed]
    [Google Scholar]
  2. Ainley D. G. . ( 2002; ). The Adélie Penguin: Bellwether of Climate Change. New York:: Columbia University Press;.
    [Google Scholar]
  3. Alexander D. J. , Manvell R. J. , Collins M. S. , Brockman S. J. , Westbury H. A. , Morgan I. , Austin F. J. . ( 1989; ). Characterization of paramyxoviruses isolated from penguins in Antarctica and sub-Antarctica during 1976–1979. . Arch Virol 109:, 135–143. [CrossRef] [PubMed]
    [Google Scholar]
  4. Altschul S. F. , Gish W. , Miller W. , Myers E. W. , Lipman D. J. . ( 1990; ). Basic local alignment search tool. . J Mol Biol 215:, 403–410.[PubMed] [CrossRef]
    [Google Scholar]
  5. Angulo M. , Carvajal-Rodríguez A. . ( 2007; ). Evidence of recombination within human alpha-papillomavirus. . Virol J 4:, 33. [CrossRef] [PubMed]
    [Google Scholar]
  6. Anisimova M. , Gascuel O. . ( 2006; ). Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. . Syst Biol 55:, 539–552. [CrossRef] [PubMed]
    [Google Scholar]
  7. Austin F. J. , Webster R. G. . ( 1993; ). Evidence of ortho- and paramyxoviruses in fauna from Antarctica. . J Wildl Dis 29:, 568–571. [CrossRef] [PubMed]
    [Google Scholar]
  8. Baker T. S. , Newcomb W. W. , Olson N. H. , Cowsert L. M. , Olson C. , Brown J. C. . ( 1991; ). Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction. . Biophys J 60:, 1445–1456. [CrossRef] [PubMed]
    [Google Scholar]
  9. Ballard G. , Toniolo V. , Ainley D. G. , Parkinson C. L. , Arrigo K. R. , Trathan P. N. . ( 2010; ). Responding to climate change: Adélie penguins confront astronomical and ocean boundaries. . Ecology 91:, 2056–2069. [CrossRef] [PubMed]
    [Google Scholar]
  10. Baumeister E. , Leotta G. , Pontoriero A. , Campos A. , Montalti D. , Vigo G. , Pecoraro M. , Savy V. . ( 2004; ). Serological evidences of influenza A virus infection in Antarctica migratory birds. . Int Congr Ser 1263:, 737–740. [CrossRef]
    [Google Scholar]
  11. Bernard H. U. . ( 2013; ). Taxonomy and phylogeny of papillomaviruses: an overview and recent developments. . Infect Genet Evol 18:, 357–361. [CrossRef] [PubMed]
    [Google Scholar]
  12. Bernard H. U. , Calleja-Macias I. E. , Dunn S. T. . ( 2006; ). Genome variation of human papillomavirus types: phylogenetic and medical implications. . Int J Cancer 118:, 1071–1076. [CrossRef] [PubMed]
    [Google Scholar]
  13. Bernard H.-U. , Burk R. D. , Chen Z. , van Doorslaer K. , zur Hausen H. , de Villiers E.-M. . ( 2010; ). Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. . Virology 401:, 70–79. [CrossRef] [PubMed]
    [Google Scholar]
  14. Boni M. F. , Posada D. , Feldman M. W. . ( 2007; ). An exact nonparametric method for inferring mosaic structure in sequence triplets. . Genetics 176:, 1035–1047. [CrossRef] [PubMed]
    [Google Scholar]
  15. Bravo I. G. , Alonso A. . ( 2007; ). Phylogeny and evolution of papillomaviruses based on the E1 and E2 proteins. . Virus Genes 34:, 249–262. [CrossRef] [PubMed]
    [Google Scholar]
  16. Carulei O. , Douglass N. , Williamson A. L. . ( 2009; ). Phylogenetic analysis of three genes of Penguinpox virus corresponding to Vaccinia virus G8R (VLTF-1), A3L (P4b) and H3L reveals that it is most closely related to Turkeypox virus, Ostrichpox virus and Pigeonpox virus. . Virol J 6:, 52. [CrossRef] [PubMed]
    [Google Scholar]
  17. Carvajal-Rodríguez A. . ( 2008; ). Detecting recombination and diversifying selection in human alpha-papillomavirus. . Infect Genet Evol 8:, 689–692. [CrossRef] [PubMed]
    [Google Scholar]
  18. Cole S. T. , Danos O. . ( 1987; ). Nucleotide sequence and comparative analysis of the human papillomavirus type 18 genome: phylogeny of papillomaviruses and repeated structure of the E6 and E7 gene products. . J Mol Biol 193:, 599–608. [CrossRef] [PubMed]
    [Google Scholar]
  19. Dayaram A. , Goldstien S. , Zawar-Reza P. , Gomez C. , Harding J. S. , Varsani A. . ( 2013; ). Identification of starling circovirus in an estuarine mollusc (Amphibola crenata) in New Zealand using metagenomic approaches. . Genome Announc 1:, e00278-13. [CrossRef] [PubMed]
    [Google Scholar]
  20. Dayaram A. , Galatowitsch M. , Harding J. S. , Argüello-Astorga G. R. , Varsani A. . ( 2014; ). Novel circular DNA viruses identified in Procordulia grayi and Xanthocnemis zealandica larvae using metagenomic approaches. . Infect Genet Evol 22:, 134–141. [CrossRef] [PubMed]
    [Google Scholar]
  21. de Villiers E. M. , Fauquet C. , Broker T. R. , Bernard H. U. , zur Hausen H. . ( 2004; ). Classification of papillomaviruses. . Virology 324:, 17–27. [CrossRef] [PubMed]
    [Google Scholar]
  22. Duffy S. , Holmes E. C. . ( 2008; ). Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus tomato yellow leaf curl virus. . J Virol 82:, 957–965. [CrossRef] [PubMed]
    [Google Scholar]
  23. Duffy S. , Holmes E. C. . ( 2009; ). Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses. . J Gen Virol 90:, 1539–1547. [CrossRef] [PubMed]
    [Google Scholar]
  24. Edgar R. C. . ( 2004; ). muscle: multiple sequence alignment with high accuracy and high throughput. . Nucleic Acids Res 32:, 1792–1797. [CrossRef] [PubMed]
    [Google Scholar]
  25. Firth C. , Charleston M. A. , Duffy S. , Shapiro B. , Holmes E. C. . ( 2009; ). Insights into the evolutionary history of an emerging livestock pathogen: porcine circovirus 2. . J Virol 83:, 12813–12821. [CrossRef] [PubMed]
    [Google Scholar]
  26. García-Vallvé S. , Alonso A. , Bravo I. G. . ( 2005; ). Papillomaviruses: different genes have different histories. . Trends Microbiol 13:, 514–521. [CrossRef] [PubMed]
    [Google Scholar]
  27. Gardner H. , Kerry K. , Riddle M. , Brouwer S. , Gleeson L. . ( 1997; ). Poultry virus infection in Antarctic penguins. . Nature 387:, 245. [CrossRef] [PubMed]
    [Google Scholar]
  28. Gibbs M. J. , Armstrong J. S. , Gibbs A. J. . ( 2000; ). Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. . Bioinformatics 16:, 573–582. [CrossRef] [PubMed]
    [Google Scholar]
  29. Gottschling M. , Bravo I. G. , Schulz E. , Bracho M. A. , Deaville R. , Jepson P. D. , Van Bressem M.-F. , Stockfleth E. , Nindl I. . ( 2011a; ). Modular organizations of novel cetacean papillomaviruses. . Mol Phylogenet Evol 59:, 34–42. [CrossRef] [PubMed]
    [Google Scholar]
  30. Gottschling M. , Göker M. , Stamatakis A. , Bininda-Emonds O. R. , Nindl I. , Bravo I. G. . ( 2011b; ). Quantifying the phylodynamic forces driving papillomavirus evolution. . Mol Biol Evol 28:, 2101–2113. [CrossRef] [PubMed]
    [Google Scholar]
  31. Grigoras I. , Timchenko T. , Grande-Pérez A. , Katul L. , Vetten H. J. , Gronenborn B. . ( 2010; ). High variability and rapid evolution of a nanovirus. . J Virol 84:, 9105–9117. [CrossRef] [PubMed]
    [Google Scholar]
  32. Guindon S. , Dufayard J. F. , Lefort V. , Anisimova M. , Hordijk W. , Gascuel O. . ( 2010; ). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. . Syst Biol 59:, 307–321. [CrossRef] [PubMed]
    [Google Scholar]
  33. Harkins G. W. , Delport W. , Duffy S. , Wood N. , Monjane A. L. , Owor B. E. , Donaldson L. , Saumtally S. , Triton G. . & other authors ( 2009; ). Experimental evidence indicating that mastreviruses probably did not co-diverge with their hosts. . Virol J 6:, 104. [CrossRef] [PubMed]
    [Google Scholar]
  34. Harkins G. W. , Martin D. P. , Christoffels A. , Varsani A. . ( 2014; ). Towards inferring the global movement of beak and feather disease virus. . Virology 450-451:, 24–33. [CrossRef] [PubMed]
    [Google Scholar]
  35. Herbst L. H. , Lenz J. , Van Doorslaer K. , Chen Z. , Stacy B. A. , Wellehan J. F. Jr , Manire C. A. , Burk R. D. . ( 2009; ). Genomic characterization of two novel reptilian papillomaviruses, Chelonia mydas papillomavirus 1 and Caretta caretta papillomavirus 1. . Virology 383:, 131–135. [CrossRef] [PubMed]
    [Google Scholar]
  36. Kane O. J. , Uhart M. M. , Rago V. , Pereda A. J. , Smith J. R. , Van Buren A. , Clark J. A. , Boersma P. D. . ( 2012; ). Avian pox in Magellanic penguins (Spheniscus magellanicus). . J Wildl Dis 48:, 790–794. [CrossRef] [PubMed]
    [Google Scholar]
  37. Katoh K. , Standley D. M. . ( 2013; ). mafft multiple sequence alignment software version 7: improvements in performance and usability. . Mol Biol Evol 30:, 772–780. [CrossRef] [PubMed]
    [Google Scholar]
  38. Kincaid A. L. , Bunton T. E. , Cranfield M. . ( 1988; ). Herpesvirus-like infection in black-footed penguins (Spheniscus demersus). . J Wildl Dis 24:, 173–175. [CrossRef] [PubMed]
    [Google Scholar]
  39. Kraberger S. , Stainton D. , Dayaram A. , Zawar-Reza P. , Gomez C. , Harding J. S. , Varsani A. . ( 2013; ). Discovery of Sclerotinia sclerotiorum hypovirulence-associated virus-1 in urban river sediments of Heathcote and Styx Rivers in Christchurch City, New Zealand. . Genome Announc 1:, e00559-13. [CrossRef] [PubMed]
    [Google Scholar]
  40. Lange C. E. , Favrot C. , Ackermann M. , Gull J. , Vetsch E. , Tobler K. . ( 2011; ). Novel snake papillomavirus does not cluster with other non-mammalian papillomaviruses. . Virol J 8:, 436. [CrossRef] [PubMed]
    [Google Scholar]
  41. Lefeuvre P. , Martin D. P. , Harkins G. , Lemey P. , Gray A. J. A. , Meredith S. , Lakay F. , Monjane A. , Lett J. M. . & other authors ( 2010; ). The spread of tomato yellow leaf curl virus from the Middle East to the world. . PLoS Pathog 6:, e1001164. [CrossRef] [PubMed]
    [Google Scholar]
  42. López-Bueno A. , Tamames J. , Velázquez D. , Moya A. , Quesada A. , Alcamí A. . ( 2009; ). High diversity of the viral community from an Antarctic lake. . Science 326:, 858–861. [CrossRef] [PubMed]
    [Google Scholar]
  43. Lyver P. O. B. , Barron M. , Barton K. J. , Ainley D. G. , Pollard A. , Gordon S. , McNeil G. , Ballard G. , Wilson P. R. . ( 2014; ). Trends in the breeding population of Adélie penguins (Pygoscelis adeliae) in the Western Ross Sea, 1981–2012: a coincidence of climate and resource extraction effects. . PLoS ONE 9:, e91188. [CrossRef]
    [Google Scholar]
  44. Martin D. , Rybicki E. . ( 2000; ). rdp: detection of recombination amongst aligned sequences. . Bioinformatics 16:, 562–563. [CrossRef] [PubMed]
    [Google Scholar]
  45. Martin D. P. , Posada D. , Crandall K. A. , Williamson C. . ( 2005; ). A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. . AIDS Res Hum Retroviruses 21:, 98–102. [CrossRef] [PubMed]
    [Google Scholar]
  46. Martin D. P. , Lemey P. , Lott M. , Moulton V. , Posada D. , Lefeuvre P. . ( 2010; ). rdp3: a flexible and fast computer program for analyzing recombination. . Bioinformatics 26:, 2462–2463. [CrossRef] [PubMed]
    [Google Scholar]
  47. Martin D. P. , Biagini P. , Lefeuvre P. , Golden M. , Roumagnac P. , Varsani A. . ( 2011; ). Recombination in eukaryotic single stranded DNA viruses. . Viruses 3:, 1699–1738. [CrossRef] [PubMed]
    [Google Scholar]
  48. McBride A. A. . ( 2013; ). The papillomavirus E2 proteins. . Virology 445:, 57–79. [CrossRef] [PubMed]
    [Google Scholar]
  49. Miller P. J. , Afonso C. L. , Spackman E. , Scott M. A. , Pedersen J. C. , Senne D. A. , Brown J. D. , Fuller C. M. , Uhart M. M. . & other authors ( 2010; ). Evidence for a new avian paramyxovirus serotype 10 detected in rockhopper penguins from the Falkland Islands. . J Virol 84:, 11496–11504. [CrossRef] [PubMed]
    [Google Scholar]
  50. Morgan I. R. , Westbury H. A. . ( 1981; ). Virological studies of Adelie penguins (Pygoscelis adeliae) in Antarctica. . Avian Dis 25:, 1019–1026. [CrossRef] [PubMed]
    [Google Scholar]
  51. Morgan I. R. , Westbury H. A. . ( 1988; ). Studies of viruses in penguins in the Vestfold Hills. . Hydrobiologia 165:, 263–269. [CrossRef]
    [Google Scholar]
  52. Morgan I. R. , Westbury H. A. , Caple I. W. , Campbell J. . ( 1981; ). A survey of virus infection in sub-Antarctic penguins on Macquarie Island, Southern Ocean. . Aust Vet J 57:, 333–335. [CrossRef] [PubMed]
    [Google Scholar]
  53. Morgan I. R. , Westbury H. A. , Campbell J. . ( 1985; ). Viral infections of little blue penguins (Eudyptula minor) along the southern coast of Australia. . J Wildl Dis 21:, 193–198. [CrossRef] [PubMed]
    [Google Scholar]
  54. Muhire B. , Martin D. P. , Brown J. K. , Navas-Castillo J. , Moriones E. , Zerbini F. M. , Rivera-Bustamante R. , Malathi V. G. , Briddon R. W. , Varsani A. . ( 2013; ). A genome-wide pairwise-identity-based proposal for the classification of viruses in the genus Mastrevirus (family Geminiviridae). . Arch Virol 158:, 1411–1424. [CrossRef] [PubMed]
    [Google Scholar]
  55. Narechania A. , Chen Z. , DeSalle R. , Burk R. D. . ( 2005a; ). Phylogenetic incongruence among oncogenic genital alpha human papillomaviruses. . J Virol 79:, 15503–15510. [CrossRef] [PubMed]
    [Google Scholar]
  56. Narechania A. , Terai M. , Burk R. D. . ( 2005b; ). Overlapping reading frames in closely related human papillomaviruses result in modular rates of selection within E2. . J Gen Virol 86:, 1307–1313. [CrossRef] [PubMed]
    [Google Scholar]
  57. Padidam M. , Sawyer S. , Fauquet C. M. . ( 1999; ). Possible emergence of new geminiviruses by frequent recombination. . Virology 265:, 218–225. [CrossRef] [PubMed]
    [Google Scholar]
  58. Park Y. M. , Kim J. H. , Gu S. H. , Lee S. Y. , Lee M. G. , Kang Y. K. , Kang S. H. , Kim H. J. , Song J. W. . ( 2012; ). Full genome analysis of a novel adenovirus from the South Polar skua (Catharacta maccormicki) in Antarctica. . Virology 422:, 144–150. [CrossRef] [PubMed]
    [Google Scholar]
  59. Phan T. G. , Kapusinszky B. , Wang C. , Rose R. K. , Lipton H. L. , Delwart E. L. . ( 2011; ). The fecal viral flora of wild rodents. . PLoS Pathog 7:, e1002218. [CrossRef] [PubMed]
    [Google Scholar]
  60. Posada D. . ( 2009; ). Selection of models of DNA evolution with jModelTest. . Methods Mol Biol 537:, 93–112. [CrossRef] [PubMed]
    [Google Scholar]
  61. Posada D. , Crandall K. A. . ( 2001; ). Evaluation of methods for detecting recombination from DNA sequences: computer simulations. . Proc Natl Acad Sci U S A 98:, 13757–13762. [CrossRef] [PubMed]
    [Google Scholar]
  62. Rector A. , Van Ranst M. . ( 2013; ). Animal papillomaviruses. . Virology 445:, 213–223. [CrossRef] [PubMed]
    [Google Scholar]
  63. Rector A. , Van Doorslaer K. , Bertelsen M. , Barker I. K. , Olberg R. A. , Lemey P. , Sundberg J. P. , Van Ranst M. . ( 2005; ). Isolation and cloning of the raccoon (Procyon lotor) papillomavirus type 1 by using degenerate papillomavirus-specific primers. . J Gen Virol 86:, 2029–2033. [CrossRef] [PubMed]
    [Google Scholar]
  64. Rector A. , Stevens H. , Lacave G. , Lemey P. , Mostmans S. , Salbany A. , Vos M. , Van Doorslaer K. , Ghim S. J. . & other authors ( 2008; ). Genomic characterization of novel dolphin papillomaviruses provides indications for recombination within the Papillomaviridae . . Virology 378:, 151–161. [CrossRef] [PubMed]
    [Google Scholar]
  65. Schulz E. , Gottschling M. , Ulrich R. G. , Richter D. , Stockfleth E. , Nindl I. . ( 2012; ). Isolation of three novel rat and mouse papillomaviruses and their genomic characterization. . PLoS ONE 7:, e47164. [CrossRef] [PubMed]
    [Google Scholar]
  66. Shah S. D. , Doorbar J. , Goldstein R. A. . ( 2010; ). Analysis of host-parasite incongruence in papillomavirus evolution using importance sampling. . Mol Biol Evol 27:, 1301–1314. [CrossRef] [PubMed]
    [Google Scholar]
  67. Shope R. E. , Hurst E. W. . ( 1933; ). Infectious papillomatosis of rabbits: with a note on the histopathology. . J Exp Med 58:, 607–624. [CrossRef] [PubMed]
    [Google Scholar]
  68. Sikorski A. , Argüello-Astorga G. R. , Dayaram A. , Dobson R. C. , Varsani A. . ( 2013a; ). Discovery of a novel circular single-stranded DNA virus from porcine faeces. . Arch Virol 158:, 283–289. [CrossRef] [PubMed]
    [Google Scholar]
  69. Sikorski A. , Dayaram A. , Varsani A. . ( 2013b; ). Identification of a novel circular DNA Virus in New Zealand fur seal (Arctocephalus forsteri) fecal matter. . Genome Announc 1:, e00558-e13. [CrossRef] [PubMed]
    [Google Scholar]
  70. Sikorski A. , Kearvell J. , Elkington S. , Dayaram A. , Argüello-Astorga G. R. , Varsani A. . ( 2013c; ). Novel ssDNA viruses discovered in yellow-crowned parakeet (Cyanoramphus auriceps) nesting material. . Arch Virol 158:, 1603–1607. [CrossRef] [PubMed]
    [Google Scholar]
  71. Sikorski A. , Massaro M. , Kraberger S. , Young L. M. , Smalley D. , Martin D. P. , Varsani A. . ( 2013; d ). Novel myco-like DNA viruses discovered in the faecal matter of various animals. . Virus Res 177:, 209–216. [CrossRef] [PubMed]
    [Google Scholar]
  72. Simpson J. T. , Wong K. , Jackman S. D. , Schein J. E. , Jones S. J. , Birol I. . ( 2009; ). ABySS: a parallel assembler for short read sequence data. . Genome Res 19:, 1117–1123. [CrossRef] [PubMed]
    [Google Scholar]
  73. Smith J. M. . ( 1992; ). Analyzing the mosaic structure of genes. . J Mol Evol 34:, 126–129. [CrossRef] [PubMed]
    [Google Scholar]
  74. Smith K. M. , Karesh W. B. , Majluf P. , Paredes R. , Zavalaga C. , Hoogesteijn Reul A. , Stetter M. , Braselton W. E. , Puche H. , Cook R. A. . ( 2008; ). Health evaluation of free-ranging Humboldt penguins (Spheniscus humboldti) in Peru. . Avian Dis 52:, 130–135. [CrossRef] [PubMed]
    [Google Scholar]
  75. Swanson M. M. , Reavy B. , Makarova K. S. , Cock P. J. , Hopkins D. W. , Torrance L. , Koonin E. V. , Taliansky M. . ( 2012; ). Novel bacteriophages containing a genome of another bacteriophage within their genomes. . PLoS ONE 7:, e40683. [CrossRef] [PubMed]
    [Google Scholar]
  76. Tachezy R. , Rector A. , Havelkova M. , Wollants E. , Fiten P. , Opdenakker G. , Jenson B. , Sundberg J. , Van Ranst M. . ( 2002; ). Avian papillomaviruses: the parrot Psittacus erithacus papillomavirus (PePV) genome has a unique organization of the early protein region and is phylogenetically related to the chaffinch papillomavirus. . BMC Microbiol 2:, 19. [CrossRef] [PubMed]
    [Google Scholar]
  77. Terai M. , Burk R. D. . ( 2002; ). Felis domesticus papillomavirus, isolated from a skin lesion, is related to canine oral papillomavirus and contains a 1.3 kb non-coding region between the E2 and L2 open reading frames. . J Gen Virol 83:, 2303–2307.[PubMed]
    [Google Scholar]
  78. Terai M. , DeSalle R. , Burk R. D. . ( 2002; ). Lack of canonical E6 and E7 open reading frames in bird papillomaviruses: Fringilla coelebs papillomavirus and Psittacus erithacus timneh papillomavirus. . J Virol 76:, 10020–10023. [CrossRef] [PubMed]
    [Google Scholar]
  79. Thomazelli L. M. , Araujo J. , Oliveira D. B. , Sanfilippo L. , Ferreira C. S. , Brentano L. , Pelizari V. H. , Nakayama C. , Duarte R. . & other authors ( 2010; ). Newcastle disease virus in penguins from King George Island on the Antarctic region. . Vet Microbiol 146:, 155–160. [CrossRef] [PubMed]
    [Google Scholar]
  80. Tornesello, M. L., Buonaguro, F. M., Meglio, A., Buonaguro, L., Beth-Giraldo, E. & Giraldo, G. (1997). Sequence variations and viral genomic state of human papillomavirus type 16 in penile carcinomas from Ugandan patients. J Gen Virol 78, 2199–2208.
  81. Trus B. L. , Buck C. B. , Cheng N. , Lowy D. R. , Steven A. C. , Schiller J. T. . ( 2005; ). Localization of the HPV-16 minor capsid protein L2 by difference imaging. . Microsc Microanal 11: (Suppl. 2), 642–643.[CrossRef]
    [Google Scholar]
  82. Tuttle A. D. , Andreadis T. G. , Frasca S. Jr , Dunn J. L. . ( 2005; ). Eastern equine encephalitis in a flock of African penguins maintained at an aquarium. . J Am Vet Med Assoc 226:, 2059–2062, 2003. [CrossRef] [PubMed]
    [Google Scholar]
  83. Van Doorslaer K. . ( 2013; ). Evolution of the Papillomaviridae . . Virology 445:, 11–20. [CrossRef] [PubMed]
    [Google Scholar]
  84. Van Doorslaer K. , Ould M’hamed Ould Sidi A. , Zanier K. , Rybin V. , Deryckère F. , Rector A. , Burk R. D. , Lienau E. K. , van Ranst M. , Travé G. . ( 2009; ). Identification of unusual E6 and E7 proteins within avian papillomaviruses: cellular localization, biophysical characterization, and phylogenetic analysis. . J Virol 83:, 8759–8770. [CrossRef] [PubMed]
    [Google Scholar]
  85. Varsani A. , van der Walt E. , Heath L. , Rybicki E. P. , Williamson A. L. , Martin D. P. . ( 2006; ). Evidence of ancient papillomavirus recombination. . J Gen Virol 87:, 2527–2531. [CrossRef] [PubMed]
    [Google Scholar]
  86. Varsani A. , Martin D. P. , Navas-Castillo J. , Moriones E. , Hernández-Zepeda C. , Idris A. , Murilo Zerbini F. , Brown J. K. . ( 2014; ). Revisiting the classification of curtoviruses based on genome-wide pairwise identity. . Arch Virol. [CrossRef] [PubMed]
    [Google Scholar]
  87. Woolford L. , Rector A. , Van Ranst M. , Ducki A. , Bennett M. D. , Nicholls P. K. , Warren K. S. , Swan R. A. , Wilcox G. E. , O’Hara A. J. . ( 2007; ). A novel virus detected in papillomas and carcinomas of the endangered western barred bandicoot (Perameles bougainville) exhibits genomic features of both the Papillomaviridae and Polyomaviridae . . J Virol 81:, 13280–13290. [CrossRef] [PubMed]
    [Google Scholar]
  88. zur Hausen H. . ( 2009a; ). Papillomaviruses in the causation of human cancers – a brief historical account. . Virology 384:, 260–265. [CrossRef] [PubMed]
    [Google Scholar]
  89. zur Hausen H. . ( 2009b; ). The search for infectious causes of human cancers: where and why. . Virology 392:, 1–10. [CrossRef] [PubMed]
    [Google Scholar]
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