Skip to content
1887

Abstract

Papillomaviruses are non-enveloped, double-stranded DNA viruses capable of infecting a wide range of vertebrates, from chondrichthyans to mammals. In this study, we report for the first time the identification and complete genome of a papillomavirus in the thornback skate (), named papillomavirus 1 (RclaPV1). The genomic sequence was determined using a metagenomic approach and subsequently confirmed by PCR. The RclaPV1 genome is 5,539 bp in length and displays the typical organization of papillomaviruses, encoding 4 core proteins on a single DNA strand: two early genes (E1 and E2) and two late genes (L1 and L2). Maximum likelihood phylogenetic analyses of the L1 and E1 genes indicate that RclaPV1 belongs to the subfamily, clustering with fish and amphibian papillomaviruses and showing closer evolutionary relationships to amphibians than to fish.

Funding
This study was supported by the:
  • Fundação para a Ciência e a Tecnologia (Award 2022.05886.CEECIND)
    • Principal Award Recipient: FabianaNeves
  • Fundação para a Ciência e a Tecnologia (Award EXPL/BIA-EVL/1045/2021)
    • Principal Award Recipient: FabianaNeves
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001541
2025-11-07
2025-12-16

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/mgen/11/11/mgen001541.html?itemId=/content/journal/mgen/10.1099/mgen.0.001541&mimeType=html&fmt=ahah

References

  1. Campo MS. Animal models of papillomavirus pathogenesis. Virus Res 2002; 89:249–261 [View Article] [PubMed]
    [Google Scholar]
  2. Frias-De-Diego A, Jara M, Escobar LE. Papillomavirus in wildlife. Front Ecol Evol 2019; 7: [View Article]
    [Google Scholar]
  3. Van Doorslaer K, Chen Z, Bernard H-U, Chan PKS, DeSalle R et al. ICTV virus taxonomy profile: Papillomaviridae. J Gen Virol 2018; 99:989–990 [View Article] [PubMed]
    [Google Scholar]
  4. Kraberger S, Austin C, Farkas K, Desvignes T, Postlethwait JH et al. Discovery of novel fish papillomaviruses: from the Antarctic to the commercial fish market. Virology 2022; 565:65–72 [View Article] [PubMed]
    [Google Scholar]
  5. Harding EF, Russo AG, Yan GJH, Mercer LK, White PA. Revealing the uncharacterised diversity of amphibian and reptile viruses. ISME Commun 2022; 2:95 [View Article] [PubMed]
    [Google Scholar]
  6. 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]
    [Google Scholar]
  7. de Villiers E-M, Fauquet C, Broker TR, Bernard H-U, zur Hausen H. Classification of papillomaviruses. Virology 2004; 324:17–27 [View Article] [PubMed]
    [Google Scholar]
  8. Finnen RL, Erickson KD, Chen XS, Garcea RL. Interactions between papillomavirus L1 and L2 capsid proteins. J Virol 2003; 77:4818–4826 [View Article] [PubMed]
    [Google Scholar]
  9. Li Y, Xiao M, Zhang Y, Li Z, Bai S et al. Identification of two novel papillomaviruses in belugas. Front Microbiol 2023; 14:1165839 [View Article]
    [Google Scholar]
  10. Rector A, Van Ranst M. Animal papillomaviruses. Virology 2013; 445:213–223 [View Article] [PubMed]
    [Google Scholar]
  11. Surján A, Fónagy E, Eszterbauer E, Harrach B, Doszpoly A. Complete genome sequence of a novel fish papillomavirus detected in farmed wels catfish (Silurus glanis). Arch Virol 2021; 166:2603–2606 [View Article] [PubMed]
    [Google Scholar]
  12. Willemsen A, Bravo IG. Origin and evolution of papillomavirus (onco)genes and genomes. Philos Trans R Soc Lond B Biol Sci 2019; 374:20180303 [View Article] [PubMed]
    [Google Scholar]
  13. Heinicke MP, Naylor GJP, Hedges S. Cartilaginous fishes (Chondrichthyes). In The Timetree of Life 2009 pp 320–327 [View Article]
    [Google Scholar]
  14. Gaigher A, Rota A, Neves F, Muñoz-Mérida A, Blasco-Aróstegui J et al. Extensive MHC class IIβ diversity across multiple loci in the small-spotted catshark (Scyliorhinus canicula). Sci Rep 2023; 13:3837 [View Article] [PubMed]
    [Google Scholar]
  15. Tan M, Redmond AK, Dooley H, Nozu R, Sato K et al. The whale shark genome reveals patterns of vertebrate gene family evolution. Elife 2021; 10:e65394 [View Article] [PubMed]
    [Google Scholar]
  16. Dill JA, Ng TFF, Camus AC. Complete sequence of the smallest polyomavirus genome, giant guitarfish (Rhynchobatus djiddensis) polyomavirus 1. Genome Announc 2016; 4:e00391-16 [View Article] [PubMed]
    [Google Scholar]
  17. Abrantes J, Varsani A, Pereira P, Maia C, Farias I et al. Identification and characterization of a polyomavirus in the thornback skate (Raja clavata). Virol J 2023; 20:190 [View Article] [PubMed]
    [Google Scholar]
  18. Armwood AR, Stilwell JM, Ng TFF, Clauss TM, Leary JH et al. A novel herpes-like virus inducing branchial lesions in a tiger shark (Galeocerdo cuvier). Vet Pathol 2022; 59:348–352 [View Article] [PubMed]
    [Google Scholar]
  19. Leibovitz L, Lebouitz SS. A viral dermatitis of the smooth dogfish, Mustelus canis (Mitchill). J Fish Dis 1985; 8:273–279 [View Article]
    [Google Scholar]
  20. Dill JA, Camus AC, Leary JH, Ng TFF. Microscopic and molecular evidence of the first elasmobranch adomavirus, the cause of skin disease in a giant guitarfish, Rhynchobatus djiddensis. mBio 2018; 9:e00185-18 [View Article] [PubMed]
    [Google Scholar]
  21. Powell AL, Camus AC, Leary JH, Miller SN, Bell CM et al. Novel adomavirus associated with proliferative skin lesions affecting the dermal denticles of a sand tiger shark (Carcharias taurus). Front Vet Sci 2024; 11:1470052 [View Article] [PubMed]
    [Google Scholar]
  22. Camus A, Dill J, McDermott A, Camus M, Fan Ng TF. Virus-associated papillomatous skin lesions in a giant guitarfish Rhynchobatus djiddensis: a case report. Dis Aquat Organ 2016; 117:253–258 [View Article] [PubMed]
    [Google Scholar]
  23. Shi M, Lin X-D, Chen X, Tian J-H, Chen L-J et al. The evolutionary history of vertebrate RNA viruses. Nature 2018; 556:197–202 [View Article] [PubMed]
    [Google Scholar]
  24. ICES ICftEotS Final Report of the Working Group on Nephrops Surveys (WGNEPS) Cadiz, Spain: 2016
    [Google Scholar]
  25. ICES ICftEotS Manual of the IBTS North Eastern Atlantic Surveys Series of ICES Survey Protocols SISP 15; 2017
    [Google Scholar]
  26. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  27. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
    [Google Scholar]
  28. Li D, Luo R, Liu C-M, Leung C-M, Ting H-F et al. MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 2016; 102:3–11 [View Article] [PubMed]
    [Google Scholar]
  29. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article] [PubMed]
    [Google Scholar]
  30. Tisza MJ, Belford AK, Domínguez-Huerta G, Bolduc B, Buck CB. Cenote-Taker 2 democratizes virus discovery and sequence annotation. Virus Evol 2021; 7:veaa100 [View Article] [PubMed]
    [Google Scholar]
  31. 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]
  32. 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]
  33. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  34. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article] [PubMed]
    [Google Scholar]
  35. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  36. Letunic I, Bork P. Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res 2024; 52:W78–W82 [View Article]
    [Google Scholar]
  37. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011; 27:1164–1165 [View Article]
    [Google Scholar]
  38. Gilchrist CLM, Chooi Y-H. clinker & clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics 2021; 37:2473–2475 [View Article]
    [Google Scholar]
  39. Buck CB, Welch N, Belford AK, Varsani A, Pastrana DV et al. Widespread horizontal gene transfer among animal viruses. bioRxiv 2024 [View Article]
    [Google Scholar]
  40. García-Vallvé S, Iglesias-Rozas JR, Alonso Á, Bravo IG. Different papillomaviruses have different repertoires of transcription factor binding sites: convergence and divergence in the upstream regulatory region. BMC Evol Biol 2006; 6:20 [View Article]
    [Google Scholar]
  41. O’Connor M, Chan SY, Bernard H-U. eds Transcription Factor Binding Sites in the Long Control Region of Genital HPVs1995
    [Google Scholar]
  42. Canuti M, Munro HJ, Robertson GJ, Kroyer ANK, Roul S et al. New insight into avian papillomavirus ecology and evolution from characterization of novel wild bird papillomaviruses. Front Microbiol 2019; 10:701 [View Article] [PubMed]
    [Google Scholar]
  43. Agius JE, Phalen DN, Rose K, Eden J-S. New insights into Sauropsid Papillomaviridae evolution and epizootiology: discovery of two novel papillomaviruses in native and invasive island geckos. Virus Evol 2019; 5:vez051 [View Article] [PubMed]
    [Google Scholar]
  44. Willemsen A, van den Boom A, Dietz J, Bilge Dagalp S, Dogan F et al. Genomic and phylogenetic characterization of ChPV2, a novel goat PV closely related to the Xi-PV1 species infecting bovines. Virol J 2020; 17:167 [View Article] [PubMed]
    [Google Scholar]
  45. Van Doorslaer K. Evolution of the Papillomaviridae. Virology 2013; 445:11–20 [View Article] [PubMed]
    [Google Scholar]
  46. Willemsen A, Bravo IG. Origin and evolution of papillomavirus (onco)genes and genomes. Phil Trans R Soc B 2019; 374:20180303 [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]
    [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. Bergvall M, Melendy T, Archambault J. The E1 proteins. Virology 2013; 445:35–56 [View Article] [PubMed]
    [Google Scholar]
  50. Ma T, Zou N, Lin BY, Chow LT, Harper JW. Interaction between cyclin-dependent kinases and human papillomavirus replication-initiation protein E1 is required for efficient viral replication. Proc Natl Acad Sci USA 1999; 96:382–387 [View Article]
    [Google Scholar]
  51. Polinas M, Cacciotto C, Zobba R, Antuofermo E, Burrai GP et al. Ovine papillomaviruses: diversity, pathogenicity, and evolution. Vet Microbiol 2024; 289:109955 [View Article] [PubMed]
    [Google Scholar]
  52. McBride AA. The papillomavirus E2 proteins. Virology 2013; 445:57–79 [View Article] [PubMed]
    [Google Scholar]
  53. Steger G, Ham J, Lefebvre O, Yaniv M. The bovine papillomavirus 1 E2 protein contains two activation domains: one that interacts with TBP and another that functions after TBP binding. EMBO J 1995; 14:329–340 [View Article] [PubMed]
    [Google Scholar]
  54. Buck CB, Day PM, Trus BL. The papillomavirus major capsid protein L1. Virology 2013; 445:169–174 [View Article] [PubMed]
    [Google Scholar]
  55. Wang JW, Roden RBS. L2, the minor capsid protein of papillomavirus. Virology 2013; 445:175–186 [View Article]
    [Google Scholar]
  56. Chen X-X, Wu W-C, Shi M. Discovery and characterization of actively replicating DNA and retro-transcribing viruses in lower vertebrate hosts based on RNA sequencing. Viruses 2021; 13:1042 [View Article]
    [Google Scholar]
  57. Olivo D, Kraberger S, Varsani A. New duck papillomavirus type identified in a mallard in Missouri, USA. Arch Virol 2024; 169:77 [View Article]
    [Google Scholar]
  58. Xavier R, Santos JL, Veríssimo A. Phylogenetic evidence for an ancestral coevolution between a major clade of coccidian parasites and elasmobranch hosts. Syst Parasitol 2018; 95:367–371 [View Article] [PubMed]
    [Google Scholar]
  59. King KM, Rajadhyaksha EV, Tobey IG, Van Doorslaer K. Synonymous nucleotide changes drive papillomavirus evolution. Tumour Virus Res 2022; 14:200248 [View Article] [PubMed]
    [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001541
Loading
/content/journal/mgen/10.1099/mgen.0.001541
Loading

Data & Media loading...

Supplements

Supplementary material 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