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Genomic sequencing of a virus representing a novel type within the species Dyopipapillomavirus 1 in an Indian River Lagoon bottlenose dolphin

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Abstract

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.

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Funding

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).

Author information

Author notes

  1. Stephen D. McCulloch & Juli D. Goldstein

    Present address: Protect Wild Dolphins Alliance, 2046 Treasure Coast Plaza, Vero Beach, FL, 32960, USA

Authors and Affiliations

  1. Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL, USA

    Galaxia Cortés-Hinojosa

  2. Department of Infectious Diseases and Immunology, College of Veterinary Medicine, University of Florida, Bldg 1379, Mowry Road, Gainesville, FL, 32611, USA

    Kuttichantran Subramaniam & Thomas B. Waltzek

  3. Department of Comparative, Diagnostic and Population Medicine, College of Veterinary Medicine, University of Florida, Gainesville, FL, USA

    James F. X. Wellehan Jr.

  4. College of Veterinary Medicine, University of Georgia, Athens, GA, USA

    Terry Fei Fan Ng

  5. Blood Systems Research Institute, San Francisco, USA

    Terry Fei Fan Ng & Eric Delwart

  6. Department of Laboratory Medicine, University of California at San Francisco, San Francisco, CA, USA

    Terry Fei Fan Ng & Eric Delwart

  7. Division of Marine Mammal Research and Conservation, Center of Marine Ecosystems Health, Harbor Branch Oceanographic Institution, Florida Atlantic University, Fort Pierce, FL, USA

    Stephen D. McCulloch, Juli D. Goldstein & Adam M. Schaefer

  8. National Oceanic and Atmospheric Administration, National Ocean Service, Center for Coastal Environmental Health and Biomolecular Research, Charleston, SC, USA

    Patricia A. Fair

  9. Department of Environmental and Radiological Health Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, USA

    John S. Reif

  10. Georgia Aquarium, 225 Baker Street, NW, Atlanta, GA, 30313, USA

    Gregory D. Bossart

  11. Division of Comparative Pathology, Miller School of Medicine, University of Miami, PO Box 016960, (R-46), Miami, FL, 33101, USA

    Gregory D. Bossart

Authors
  1. Galaxia Cortés-Hinojosa
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  2. Kuttichantran Subramaniam
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  3. James F. X. Wellehan Jr.
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  4. Terry Fei Fan Ng
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  6. Stephen D. McCulloch
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  7. Juli D. Goldstein
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  8. Adam M. Schaefer
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  9. Patricia A. Fair
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  11. Gregory D. Bossart
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  12. Thomas B. Waltzek
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Corresponding author

Correspondence to Thomas B. Waltzek.

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Conflict of interest

All the authors declare that they have no conflict of interest.

Ethical approval

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.

Additional information

Handling Editor: Zhongjie Shi.

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Fig. S1

Genetic comparison of the L1 gene of a novel type of Dyopipapillomavirus 1 from a bottlenose dolphin (Tursiops truncatus papillomavirus 8; TtPV8) to those of representatives of 49 accepted type species in the family Papillomaviridae. Values are expressed as percent nucleotide sequence identity. See Table S3 for PV abbreviations. (PDF 823 kb)

Supplementary material 2 (DOC 55 kb)

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Supplementary material 4 (DOC 112 kb)

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Cortés-Hinojosa, G., Subramaniam, K., Wellehan, J.F.X. et al. Genomic sequencing of a virus representing a novel type within the species Dyopipapillomavirus 1 in an Indian River Lagoon bottlenose dolphin. Arch Virol 164, 767–774 (2019). https://doi.org/10.1007/s00705-018-04117-5

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  • DOI: https://doi.org/10.1007/s00705-018-04117-5

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