Detection of Cetacean Poxvirus in Peruvian Common Bottlenose Dolphins (Tursiops truncatus) Using a Pan-Poxvirus PCR
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Schoch, C.L.; Ciufo, S.; Domrachev, M.; Hotton, C.L.; Kannan, S.; Khovanskaya, R.; Leipe, D.; McVeigh, R.; O’Neill, K.; Robbertse, B.; et al. NCBI Taxonomy: A comprehensive update on curation, resources and tools. Database 2020, 2020, baaa062. [Google Scholar] [CrossRef] [PubMed]
- Haller, S.L.; Peng, C.; McFadden, G.; Rothenburg, S. Poxviruses and the evolution of host range and virulence. Infect. Genet. Evol. 2013, 21, 15–40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Duignan, P.J.; Van Bressem, M.F.; Cortés-Hinojosa, G.; Kennedy-Stoskopf, S. Viruses of Marine Mammals. In CRC Handbook of Marine Mammal Medicine: Health, Disease, and Rehabilitation, 3rd ed.; Dierauf, L.A., Gulland, F.M.D., Eds.; Taylor and Francis Publishers: Boca Raton, FL, USA, 2018. [Google Scholar]
- Osterhaus, A.D.M.E.; Broeders, H.W.J.; Visser, I.K.G.; Teppema, J.S.; Vedder, E.J. Isolation of an orthopoxvirus from pox-like lesions of a grey seal (Halichoerus grypus). Vet. Rec. 1990, 127, 91–92. [Google Scholar] [PubMed]
- Burek, K.A.; Beckmen, K.; Gelatt, T.; Fraser, W.; Bracht, A.J.; Smolarek, K.A.; Romero, C.H. Poxvirus Infection of Steller Sea Lions (Eumetopias jubatus) in Alaska. J. Wildl. Dis. 2005, 41, 745–752. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jacob, J.M.; Subramaniam, K.; Tu, S.-L.; Nielsen, O.; Tuomi, P.A.; Upton, C.; Waltzek, T.B. Complete genome sequence of a novel sea otterpox virus. Virus Genes 2018, 54, 756–767. [Google Scholar] [CrossRef]
- Bracht, A.J.; Brudek, R.L.; Ewing, R.Y.; Manire, C.A.; Burek, K.A.; Rosa, C.; Beckmen, K.B.; Maruniak, J.E.; Romero, C.H. Genetic identification of novel poxviruses of cetaceans and pinnipeds. Arch. Virol. 2006, 151, 423–438. [Google Scholar] [CrossRef]
- Blacklaws, B.A.; Gajda, A.M.; Tippelt, S.; Jepson, P.D.; Deaville, R.; Van Bressem, M.-F.; Pearce, G.P. Molecular Characterization of Poxviruses Associated with Tattoo Skin Lesions in UK Cetaceans. PLoS ONE 2013, 8, e71734. [Google Scholar] [CrossRef]
- Rodrigues, T.C.; Subramaniam, K.; Varsani, A.; McFadden, G.; Schaefer, A.M.; Bossart, G.D.; Romero, C.H.; Waltzek, T.B. Genome characterization of cetaceanpox virus from a managed Indo-Pacific bottlenose dolphin (Tursiops aduncus). Virus Res. 2020, 278, 197861. [Google Scholar] [CrossRef]
- Geraci, J.R.; Hicks, B.D.; St Aubin, D.J. Dolphin pox: A skin disease of cetaceans. Can. J. Comp. Med. 1979, 43, 399–404. [Google Scholar]
- Van Bressem, M.F.; Van Waerebeek, K. Epidemiology of Poxvirus in Small Cetaceans from the Eastern South Pacific. Mar. Mammal. Sci. 1996, 12, 371–382. [Google Scholar] [CrossRef]
- Van Bressem, M.F.; Raga, J.A.; Di Guardo, G.; Jepson, P.D.; Duignan, P.J.; Siebert, U.; Van Waerebeek, K. Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis. Aquat. Org. 2009, 86, 143–157. [Google Scholar] [CrossRef] [PubMed]
- Barnett, J.; Dastjerdi, A.; Davison, N.; Deaville, R.; Everest, D.; Peake, J.; Finnegan, C.; Jepson, P.; Steinbach, F. Identification of Novel Cetacean Poxviruses in Cetaceans Stranded in South West England. PLoS ONE 2015, 10, e0124315. [Google Scholar] [CrossRef] [PubMed]
- Fiorito, C.; Palacios, C.; Golemba, M.; Bratanich, A.; Argüelles, M.; Fazio, A.; Bertellotti, M.; Lombardo, D. Identification, molecular and phylogenetic analysis of poxvirus in skin lesions of southern right whale. Dis. Aquat. Org. 2015, 116, 157–163. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sacristán, C.; Esperón, F.; Marigo, J.; Ewbank, A.C.; de Carvalho, R.R.; Groch, K.R.; de Castilho, P.V.; Sánchez-Sarmiento, A.M.; Costa-Silva, S.; Ferreira-Machado, E.; et al. Molecular identification and microscopic characterization of poxvirus in a Guiana dolphin and a common bottlenose dolphin, Brazil. Dis. Aquat. Org. 2018, 130, 177–185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanino, G.P.; Van Waerebeek, K.; Van Bressem, M.F.; Pastene, L.A. A preliminary note on population structure in eastern South Pacific common bottlenose dolphins, Tursiops truncatus. J. Cetacean. Res. Manag. 2005, 7, 65. [Google Scholar]
- Van Bressem, M.F.; Van Waerebeek, K.; Reyes, J.C.; Dekegel, D.; Pastoret, P.P. Evidence of Poxvirus in Dusky Dolphin (Lagenorhynchus obscurus) and Burmeister’s Porpoise (Phocoena spinipinnis) from Coastal Peru. J. Wildl. Dis. 1993, 29, 109–113. [Google Scholar] [CrossRef] [Green Version]
- Van Bressem, M.F.; Van Waerebeek, K.; Bennett, M. Orthopoxvirus neutralising antibodies in small cetaceans from the Southeast Pacific. Lat. Am. J. Aquat. Mamm. 2006, 5, 49–54. [Google Scholar] [CrossRef]
- Luciani, L.; Inchauste, L.; Ferraris, O.; Charrel, R.; Nougairède, A.; Piorkowski, G.; Peyrefitte, C.; Bertagnoli, S.; de Lamballerie, X.; Priet, S. A novel and sensitive real-time PCR system for universal detection of poxviruses. Sci. Rep. 2021, 11, 1798, Erratum in 2022, 12, 5961. [Google Scholar] [CrossRef]
- Van Waerebeek, K.; Reyes, J. Post-Ban Small Cetacean Takes off Peru: A Review. In Report of the International Whaling Commission; International Whaling Commission: Cambridge, UK, 1994; pp. 503–519. [Google Scholar]
- Upton, C.; Slack, S.; Hunter, A.L.; Ehlers, A.; Roper, R.L. Poxvirus Orthologous Clusters: Toward Defining the Minimum Essential Poxvirus Genome. J. Virol. 2003, 77, 7590–7600. [Google Scholar] [CrossRef] [Green Version]
- Kulesh, D.A.; Baker, R.O.; Loveless, B.M.; Norwood, D.; Zwiers, S.H.; Mucker, E.; Hartmann, C.; Herrera, R.; Miller, D.; Christensen, D.; et al. Smallpox and pan -Orthopox Virus Detection by Real-Time 3′-Minor Groove Binder TaqMan Assays on the Roche LightCycler and the Cepheid Smart Cycler Platforms. J. Clin. Microbiol. 2004, 42, 601–609. [Google Scholar] [CrossRef] [Green Version]
- Nitsche, A.; Büttner, M.; Wilhelm, S.; Pauli, G.; Meyer, H. Real-Time PCR Detection of Parapoxvirus DNA. Clin. Chem. 2006, 52, 316–319. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thompson, J.D.; Higgins, D.G.; Gibson, T.J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22, 4673–4680. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cocumelli, C.; Fichi, G.; Marsili, L.; Senese, M.; Cardeti, G.; Cersini, A.; Ricci, E.; Garibaldi, F.; Scholl, F.; Di Guardo, G.; et al. Cetacean Poxvirus in Two Striped Dolphins (Stenella coeruleoalba) Stranded on the Tyrrhenian Coast of Italy: Histopathological, Ultrastructural, Biomolecular, and Ecotoxicological Findings. Front. Veter. Sci. 2018, 5, 219. [Google Scholar] [CrossRef]
- Tamura, K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol. Biol. Evol. 1992, 9, 678–687. [Google Scholar] [CrossRef] [Green Version]
- Van Waerebeek, K.; Reyes, J.C.; Read, A.J.; McKinnon, J.S. Preliminary Observations of Bottlenose Dolphins from the Pacific Coast of South America. In The Bottlenose Dolphin; Leatherwood, S., Reeves, R.R., Eds.; Elsevier: Amsterdam, The Netherlands, 1990; pp. 143–154. [Google Scholar] [CrossRef]
- Koshiba, M.; Ogawa, K.; Hamazaki, S.; Sugiyama, T.; Ogawa, O.; Kitajima, T. The Effect of Formalin Fixation on DNA and the Extraction of High-molecular-weight DNA from Fixed and Embedded Tissues. Pathol. Res. Pract. 1993, 189, 66–72. [Google Scholar] [CrossRef]
- Babkin, I.V.; Babkina, I.N. Molecular Dating in the Evolution of Vertebrate Poxviruses. Intervirology 2011, 54, 253–260. [Google Scholar] [CrossRef] [Green Version]
- Lefkowitz, E.J.; Wang, C.; Upton, C. Poxviruses: Past, present and future. Virus Res. 2006, 117, 105–118. [Google Scholar] [CrossRef]
- Hughes, A.L.; Irausquin, S.; Friedman, R. The evolutionary biology of poxviruses. Infect. Genet. Evol. 2010, 10, 50–59. [Google Scholar] [CrossRef] [Green Version]
Sample | Species | Year | Locality | Conservation | EM | Pan-Poxvirus | |
---|---|---|---|---|---|---|---|
AGG-574 | Long-beaked common dolphin | Delphinus cf. capensis | 1991 | Ancon | GA | ND | Neg |
MFB-195 | Long-beaked common dolphin | Delphinus cf. capensis | 1993 | Cerro Azul | Formalin | ND | Neg |
MFB-297 | Long-beaked common dolphin | Delphinus cf. capensis | 1993 | Cerro Azul | GA | ND | Neg |
MFB-364 | Short-finned pilot whale | Globicephala macrorhynchus | 1993 | Cerro Azul | DMSO | ND | Neg |
MFB-001 | Dusky dolphin | Lagenorhynchus obscurus | 1989 | Pucusana | Formalin | Poxvirus | Neg |
KVW-1899 | Dusky dolphin | Lagenorhynchus obscurus | 1989 | Pucusana | Formalin | ND | Neg |
AGG-580 | Dusky dolphin | Lagenorhynchus obscurus | 1991 | Ancon | GA | ND | Neg |
AGG-663 | Dusky dolphin | Lagenorhynchus obscurus | 1992 | Ancon | GA | ND | Neg |
MFB-146 | Dusky dolphin | Lagenorhynchus obscurus | 1993 | Cerro Azul | GA | ND | Neg |
KVW-1864 | Burmeister’s porpoise | Phocoena spinipinnis | 1989 | Pucusana | Formalin | ND | Neg |
KVW-1863 | Burmeister’s porpoise | Phocoena spinipinnis | 1989 | Pucusana | Formalin | ND | Neg |
KVW-2283 | Burmeister’s porpoise | Phocoena spinipinnis | 1990 | Pucusana | Formalin | Poxvirus | Neg |
KOS-83 | Burmeister’s porpoise | Phocoena spinipinnis | 1993 | Cerro Azul | Formalin | ND | Neg |
KVW-2427 | Burmeister’s porpoise | Phocoena spinipinnis | 1995 | San Jose | Formalin | ND | Neg |
MFB-465 | Common bottlenose dolphin | Tursiops truncatus | 1993 | Cerro Azul | DMSO | ND | 21CT |
MFB-187 | Common bottlenose dolphin | Tursiops truncatus | 1993 | Cerro Azul | GA | Poxvirus | 16CT |
Species | Scientific Name | Location | Sample type | Dna Polymerase Genbank # | Dna Topoisomerase Genbank # | References | Clade |
---|---|---|---|---|---|---|---|
bowhead whale | B. mysticetus | USA (Alaska) | Killed | AY846759 | AY846760 | [7] | CePV-2 |
southern right whale | E. australis | Argentina | stranded | KM000064 | KM000065 | [14] | CePV-2 |
common dolphin | D. delphis | UK (Cornwall) | stranded | KC409046 | KC409060 | [8] | CePV-1 |
common dolphin | D. delphis | UK (Cornwall) | stranded | JN654440 | NA | [13] | CePV-1 |
common dolphin | D. delphis | UK (Cornwall) | stranded | JN654441/42 | NA | [13] | CePV-1 |
common dolphin | D. delphis | UK (Cornwall) | stranded | JN654443 | NA | [13] | CePV-1 |
common dolphin | D. delphis | UK (Cornwall) | stranded | JX401226 | NA | [13] | CePV-1 |
rough-toothed dolphin | S. bredanensis | USA (FL) | stranded | AY463004 | AY952949 | [7] | CePV-1 |
rough-toothed dolphin | S. bredanensis | USA (FL) | stranded | DQ071862 | DQ071863 | [7] | CePV-1 |
striped dolphin | S. coeruleoalba | UK (Dorset) | stranded | KC409037 | KC409051 | [8] | CePV-1 |
striped dolphin | S. coeruleoalba | USA (FL) | stranded | DQ071860 | DQ071861 | [7] | CePV-1 |
striped dolphin | S. coeruleoalba | UK (Cornwall) | stranded | JN654445 | NA | [13] | CePV-1 |
striped dolphin | S. coeruleoalba | UK (Dorset) | stranded | KC409038 | KC409052 | [8] | CePV-1 |
striped dolphin | S. coeruleoalba | Italy (Toscana) | stranded | KY652339 | NA | [26] | CePV-1 |
striped dolphin | S. coeruleoalba | Italy (Lazio) | stranded | KY652340 | NA | [26] | CePV-1 |
striped dolphin | S. coeruleoalba | Spain (Mediterranean) | stranded | MH005249 | NA | [15] | CePV-1 |
guiana dolphin | S. guianensis | Brazil (Rio de Janeiro) | stranded | MF458199 | MF458200 | [15] | CePV-1 |
indo-pacific bottlenose dolphin | T. aduncus | Hong Kong | captive | MN653921 | MN653921 | [9] | CePV-TA |
indo-pacific bottlenose dolphin | T. aduncus | Hong Kong | captive | DQ071856 | DQ071857 | [7] | CePV-1 |
common bottlenose dolphin | T. truncatus | Brazil (Santa Catarina) | stranded | KU726612 | KU726611 | [15] | CePV-1 |
common bottlenose dolphin | T. truncatus | USA (FL) | stranded | AY952950 | AY952951 | [7] | CePV-1 |
common bottlenose dolphin | T. truncatus | USA (FL) | NA | DQ071858 | DQ071859 | [7] | CePV-1 |
harbor porpoise | P. phocoena | UK (Humberside) | stranded | KC409047 | KC409064 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Dorset) | stranded | KC409045 | KC409059 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (West Sussex) | stranded | KC409043 | KC409057 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Devon) | stranded | KC409044 | KC409058 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Humberside) | stranded | KC409042 | KC409056 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Humberside) | stranded | KC409041 | KC409055 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Humberside) | stranded | KC409040 | KC409054 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Kent) | stranded | KC409039 | KC409053 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Northumberland) | stranded | KC409036 | KC409050 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Humberside) | stranded | Not used | KC409061 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Humberside) | stranded | Not used | KC409062 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Humberside) | stranded | KC409049 | KC409063 | [8] | CePV-1 |
harbor porpoise | P. phocoena | UK (Cornwall) | stranded | KC242457 | NA | [13] | CePV-1 |
harbor porpoise | P. phocoena | UK (Cornwall) | stranded | KC242458 | NA | [13] | CePV-1 |
harbor porpoise | P. phocoena | UK (Cornwall) | stranded | KC242459 | NA | [13] | CePV-1 |
harbor porpoise | P. phocoena | UK (Cornwall) | stranded | JN654444 | NA | [13] | CePV-1 |
harbor porpoise | P. phocoena | UK (Cornwall) | stranded | JX401224 | NA | [13] | CePV-1 |
harbor porpoise | P. phocoena | UK (Cornwall) | stranded | JX401225 | NA | [13] | CePV-1 |
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Luciani, L.; Piorkowski, G.; De Lamballerie, X.; Van Waerebeek, K.; Van Bressem, M.-F. Detection of Cetacean Poxvirus in Peruvian Common Bottlenose Dolphins (Tursiops truncatus) Using a Pan-Poxvirus PCR. Viruses 2022, 14, 1850. https://doi.org/10.3390/v14091850
Luciani L, Piorkowski G, De Lamballerie X, Van Waerebeek K, Van Bressem M-F. Detection of Cetacean Poxvirus in Peruvian Common Bottlenose Dolphins (Tursiops truncatus) Using a Pan-Poxvirus PCR. Viruses. 2022; 14(9):1850. https://doi.org/10.3390/v14091850
Chicago/Turabian StyleLuciani, Léa, Géraldine Piorkowski, Xavier De Lamballerie, Koen Van Waerebeek, and Marie-Françoise Van Bressem. 2022. "Detection of Cetacean Poxvirus in Peruvian Common Bottlenose Dolphins (Tursiops truncatus) Using a Pan-Poxvirus PCR" Viruses 14, no. 9: 1850. https://doi.org/10.3390/v14091850