Genomic sequencing of a virus representing a novel type within the species Dyopipapillomavirus 1 in an Indian River Lagoon bottlenose dolphin
Fecal samples collected from free-ranging Atlantic bottlenose dolphins (BDs) in the Indian River Lagoon of Florida were processed for viral discovery using a next-generation sequencing (NGS) approach. A 693-bp contig identified in the NGS data was nearly identical to the partial L1 gene sequence of a papillomavirus (PV) previously found in a penile papilloma in a killer whale (Orcinus orca). Based on this partial bottlenose dolphin papillomavirus (BDPV) sequence, a nested inverse PCR and primer-walking strategy was employed to generate the complete genome sequence. The full BDPV genome consisted of 7299 bp and displayed a typical PV genome organization. The BDPV E6 protein contained a PDZ-binding motif, which has been shown to be involved in carcinogenic transformation involving high-risk genital human PVs. Screening of 12 individual fecal samples using a specific endpoint PCR assay revealed that the feces from a single female BD displaying a genital papilloma was positive for the BDPV. Genetic analysis indicated that this BDPV (Tursiops truncatus papillomavirus 8; TtPV8) is a new type of Dyopipapillomavirus 1, previously sequenced from an isolate obtained from a penile papilloma in a harbor porpoise (Phocoena phocoena). Although only a partial L1 sequence has been determined for a PV detected in a killer whale genital papilloma, our finding of a nearly identical sequence in an Atlantic BD may indicate that members of this viral species are capable of host jumping. Future work is needed to determine if this virus is a high-risk PV that is capable of inducing carcinogenic transformation and whether it poses a significant health risk to wild delphinid populations.
This study was partially funded by Florida Atlantic University (award no. 00086229), the Georgia Aquarium (award no. 03184), and the Florida Fish and Wildlife Conservation Commission (award no. 00126905).
Compliance with ethical standards
Conflict of interest
All the authors declare that they have no conflict of interest.
All animal procedures were reviewed and approved by the Institutional Animal Care and Use Committee at the University of Florida (IACUC Protocol no. 201508900). BD samples used in this study were collected under US National Marine Fisheries Service Scientific Research Permit no. 14352.
- 1.Bernard HU, Burk RD, DeVilliers EM, zur Hausen H (2012) Papillomaviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: ninth report of the international committee on taxonomy of viruses. Elsevier Academic Press, New York, pp 235–248Google Scholar
- 2.Burk R, Chen Z, van Doorslaer K, Bernard H-U, Chan PKS, Desalle R, Dillner J, Forslund O, Haga T, McBride A, Villa LL (2015) ICTV taxonomic proposal 2015.014a-atD.A.v2.Papillomaviridae_10gen. Creation of 21 new species and 10 new genera in the family Papillomaviridae. https://talk.ictvonline.org/files/ictv_official_taxonomy_updates_since_the_8th_report/m/animal-dna-viruses-and-retroviruses/5818. Accessed 12 Dec 2017
- 11.Rector A, Bossart GD, Ghim SJ, Sundberg JP, Jenson AB, Van Ranst M (2004) Characterization of a novel close-to-root papillomavirus from a Florida manatee by using multiply primed rolling-circle amplification: Trichechus manatus latirostris papillomavirus type 1. J Virol 78:12698–12702CrossRefGoogle Scholar
- 13.Ghim SJ, Joh J, Mignucci-Giannoni AA, Rivera-Guzmán AL, Falcón-Matos L, Alsina-Guerrero MM, Rodríguez-Villanueva M, Jenson AB, Bossart GD (2015) Genital papillomatosis associated with two novel mucosotropic papillomaviruses from a Florida manatee (Trichechus manatus latirostris). Aquat Mamm 40:195–200CrossRefGoogle Scholar
- 19.Van Bressem MF, Cassonnet P, Rector A, Desaintes C, Van Waerebeek K, Alfaro-Shigueto J, Van Ranst M, Orth G (2007) Genital warts in Burmeister’s porpoises: characterization of Phocoena spinipinnis papillomavirus type 1 (PsPV-1) and evidence for a second, distantly related PsPV. J Gen Virol 88:1928–1933CrossRefGoogle Scholar
- 23.Rector A, Stevens H, Lacave G, Lemey P, Mostmans S, Salbany A, Vos M, Van Doorslaer K, Ghim SJ, Rehtanz M, Bossart GD, Jenson AB, Van Ranst M (2008) Genomic characterization of novel dolphin papillomaviruses provides indications for recombination within the Papillomaviridae. Virology 378:151–161CrossRefGoogle Scholar
- 25.Ng TF, Chen LF, Zhou Y, Shapiro B, Stiller M, Heintzman PD, Varsani A, Kondov NO, Wong W, Deng X, Andrews TD, Moorman BJ, Meulendyk T, MacKay G, Gilbertson RL, Delwart E (2014) Preservation of viral genomes in 700-y-old caribou feces from a subarctic ice patch. Proc Natl Acad Sci 111:16842–16847CrossRefGoogle Scholar
- 37.Garcia-Perez R, Ibanez C, Godínez JM, Aréchiga N, Garin I, Pérez-Suárez G, de Paz O, Juste J, Echevarría JE, Bravo IG (2014) Novel papillomaviruses in free-ranging Iberian bats: no virus-host co-evolution, no strict host specificity, and hints for recombination. Genome Biol Evol 6:94–104CrossRefGoogle Scholar
- 39.Herzing DL, Elliser CR (2013) Directionality of sexual activities during mixed-species encounters between Atlantic spotted dolphins (Stenella frontalis) and bottlenose dolphins (Tursiops truncatus). Int J Comp Psychol 26:124–134Google Scholar