Molecular evidence for horizontal transmission of chelonid alphaherpesvirus 5 at green turtle (Chelonia mydas) foraging grounds in Queensland, Australia
Autoři:
K. Jones aff001; G. Burgess aff001; A. M. Budd aff002; R. Huerlimann aff002; N. Mashkour aff001; E. Ariel aff001
Působiště autorů:
College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Queensland, Australia
aff001; Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Queensland, Australia
aff002; Centre for Tropical Water and Aquatic Ecosystem Research, James Cook University, Townsville, Queensland, Australia
aff003
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0227268
Souhrn
Fibropapillomatosis (FP) is a marine turtle disease recognised by benign tumours on the skin, eyes, shell, oral cavity and/or viscera. Despite being a globally distributed disease that affects an endangered species, research on FP and its likely causative agent chelonid alphaherpesvirus 5 (ChHV5) in Australia is limited. Here we present improved molecular assays developed for detection of ChHV5, in combination with a robust molecular and phylogenetic analysis of ChHV5 variants. This approach utilised a multi-gene assay to detect ChHV5 in all FP tumors sampled from 62 marine turtles found at six foraging grounds along the Great Barrier Reef. Six distinct variants of ChHV5 were identified and the distribution of these variants was associated with host foraging ground. Conversely, no association between host genetic origin and ChHV5 viral variant was found. Together this evidence supports the hypothesis that marine turtles undergo horizontal transmission of ChHV5 at foraging grounds and are unlikely to be contracting the disease at rookeries, either during mating or vertically from parent to offspring.
Klíčová slova:
Haplotypes – Sequence analysis – Sequence alignment – Phylogenetic analysis – DNA sequence analysis – Sequence databases – Foraging – Turtles
Zdroje
1. Jones K, Ariel E, Burgess G, Read M. A review of fibropapillomatosis in Green turtles (Chelonia mydas). The Veterinary Journal. 2016;212:48–57. doi: 10.1016/j.tvjl.2015.10.041 27256025
2. Herbst LH. Fibropapillomatosis of marine turtles. Annual Review of Fish Diseases. 1994;4:389–425. doi: 10.1016/0959-8030(94)90037-X
3. Flint M, Limpus CJ, Patterson-Kane JC, Murray PJ, Mills PC. Corneal Fibropapillomatosis in Green Sea Turtles (Chelonia mydas) in Australia. Journal of Comparative Pathology. 2010;142(4):341–6. doi: 10.1016/j.jcpa.2009.10.012 19954789
4. Work TM, Balazs GH, Rameyer RA, Morris RA. Retrospective pathology survey of green turtles Chelonia mydas with fibropapillomatosis in the Hawaiian Islands, 1993–2003. Diseases of aquatic organisms. 2004;62(1–2):163–76. doi: 10.3354/dao062163 15648843
5. Aguirre AA, Balazs GH, Spraker TR, Gross TS. Adrenal and Hematological Responses to Stress in Juvenile Green Turtles (Chelonia mydas) with and without Fibropapillomas. Physiological Zoology. 1995;68(5):831–54.
6. Work TM, Rameyer RA, Balazs GH, Cray C, Chang SP. Immune status of free-ranging green turtles with fibropapillomatosis from Hawaii. Journal of wildlife diseases. 2001;37(3):574. doi: 10.7589/0090-3558-37.3.574 11504232
7. Jacobson ER, Buergelt C, Williams B, Harris RK. Herpesvirus in cutaneous fibropapillomas of the green turtle Chelonia mydas. Diseases of Aquatic Organisms. 1991;12:1–6. doi: 10.3354/dao012001
8. Jacobson ER, Mansell JL, Sundberg JP, Hajjar L, Reichmann ME, Ehrhart LM, et al. Cutaneous fibropapillomas of green turtles (Chelonia mydas). Journal of Comparative Pathology. 1989;101(1):39–52. doi: 10.1016/0021-9975(89)90075-3 2677067
9. Herbst LH, Jacobson ER, Moretti R, Brown T, Sundberg JP, Klein PA. Experimental transmission of green turtle fibropapillomatosis using cell-free tumor extracts. Diseases of Aquatic Organisms. 1995;22:1–12. doi: 10.3354/dao022001
10. Work TM, Dagenais J, Weatherby TM, Balazs GH, Ackermannd M. In vitro replication of chelonid herpesvirus 5 in organotypic skin cultures from Hawaiian green turtles (Chelonia mydas). Journal of Virology. 2017;91(17). doi: 10.1128/JVI.00404-17 28615209
11. Lackovich JK, Jacobson ER, Curry SS, Klein PA, Brown DR, Homer BL, et al. Association of herpesvirus with fibropapillomatosis of the green turtle Chelonia mydas and the loggerhead turtle Caretta caretta in Florida. Diseases of aquatic organisms. 1999;37(2):89–97. doi: 10.3354/dao037089 10494499
12. Lu Y, Wang Y, Yu Q, Aguirre AA, Balazs GH, Nerurkar VR, et al. Detection of herpesviral sequences in tissues of green turtles with fibropapilloma by polymerase chain reaction. Archives of virology. 2000;145(9):1885–93. doi: 10.1007/s007050070063 11043948
13. Lu YA, Wang Y, Aguirre AA, Zhao ZS, Liu CY, Nerurkar VR, et al. RT-PCR detection of the expression of the polymerase gene of a novel reptilian herpesvirus in tumor tissues of green turtles with fibropapilloma. Archives of virology. 2003;148(6):1155–63. doi: 10.1007/s00705-002-0970-8 12756620
14. Page-Karjian A, Norton TM, Ritchie B, Brown C, Mancia C, Jackwood M, et al. Quantifying chelonid herpesvirus 5 in symptomatic and asymptomatic rehabilitating green sea turtles. Endangered Species Research. 2015;28(2):135–46. doi: 10.3354/esr00687
15. Page-Karjian A, Torres F, Zhang J, Rivera S, Diez C, Moore PA, et al. Presence of chelonid fibropapilloma-associated herpesvirus in tumored and non-tumored green turtles, as detected by polymerase chain reaction, in endemic and non-endemic aggregations, Puerto Rico. SpringerPlus. 2012;1(1):1–8. doi: 10.1186/2193-1801-1-35 23961364
16. Quackenbush SL, Aguirre AA, Spraker TR, Horrocks JA, Vermeer LA, Balazs GH, et al. Quantitative analysis of herpesvirus sequences from normal tissue and fibropapillomas of marine turtles with real-time PCR. Virology. 2001;287(1):105–11. doi: 10.1006/viro.2001.1023 11504546
17. Quackenbush SL, Bowser PR, Work TM, Balazs GH, Casey RN, Casey JW, et al. Three Closely Related Herpesviruses Are Associated with Fibropapillomatosis in Marine Turtles. Virology. 1998;246(2):392–9. doi: 10.1006/viro.1998.9207 9657957
18. Nigro O, Alonso Aguirre A, Lu Y. Nucleotide sequence of an ICP18.5 assembly protein (UL28) gene of green turtle herpesvirus pathogenically associated with green turtle fibropapilloma. Journal of virological methods. 2004;120(1):107–12. doi: 10.1016/j.jviromet.2004.04.011 15234815
19. Nigro O, Yu G, Aguirre AA, Lu Y. Sequencing and characterization of the full-length gene encoding the single-stranded DNA binding protein of a novel Chelonian herpesvirus. Archives of virology. 2004;149(2):337–47. doi: 10.1007/s00705-003-0204-8 14745599
20. Yu Q, Hu N, Lu Y, Nerurkar VR, Yanagihara R. Rapid acquisition of entire DNA polymerase gene of a novel herpesvirus from green turtle fibropapilloma by a genomic walking technique. Journal of virological methods. 2001;91(2):183–95. doi: 10.1016/s0166-0934(00)00267-6 11164500
21. Yu Q, Lu Y, Nerurkar VR, Yanagihara R. Amplification and analysis of DNA flanking known sequences of a novel herpesvirus from green turtles with fibropapilloma Brief report. Archives of virology. 2000;145(12):2669. doi: 10.1007/s007050070015 11205112
22. Alfaro-Nunez A, Bertelsen MF, Bojesen AM, Rasmussen I, Zepeda-Mendoza L, Olsen MT, et al. Global distribution of Chelonid fibropapilloma-associated herpesvirus among clinically healthy sea turtles. BMC Evolutionary Biology. 2014;14(1). doi: 10.1186/s12862-014-0206-z 25342462
23. Rodenbusch CR, Baptistotte C, Werneck MR, Pires TT, Melo MTD, de Ataíde MW, et al. Fibropapillomatosis in green turtles Chelonia mydas in Brazil: characteristics of tumors and virus. Diseases of aquatic organisms. 2014;111(3):207–17. doi: 10.3354/dao02782 25320033
24. Patrício AR, Herbst LH, Duarte A, Vélez-Zuazo X, Santos Loureiro N, Pereira N, et al. Global phylogeography and evolution of chelonid fibropapilloma-associated herpesvirus. Journal of general virology. 2012;93:1035. doi: 10.1099/vir.0.038950-0 22258862
25. Cardenas DM, Cucalon RV, Medina-Magues LG, Jones K, Aleman RA, Alfaro-Nunez A, et al. Fibropapillomatosis in a Green Sea Turtle (Chelonia mydas) from the Southeastern Pacific. J Wildl Dis. 2018;In-Press. Epub 2018/08/11. doi: 10.7589/2017-12-295 30096036.
26. Ene A, Su M, Lemaire S, Rose C, Schaff S, Moretti R, et al. Distribution of chelonid fibropapillomatosis-associated herpesvirus variants in Florida: molecular genetic evidence for infection of turtles following recruitment to neritic developmental habitats. Journal of wildlife diseases. 2005;41(3):489. doi: 10.7589/0090-3558-41.3.489 16244058
27. Herbst L, Ene A, Su M, Desalle R, Lenz J. Tumor outbreaks in marine turtles are not due to recent herpesvirus mutations. Current Biology. 2004;14(17):R697–R9. doi: 10.1016/j.cub.2004.08.040 15341757
28. Ariel E, Nainu F, Jones K, Juntunen K, Bell I, Gaston J, et al. Phylogenetic Variation of Chelonid Alphaherpesvirus 5 (ChHV5) in Populations of Green Turtles Chelonia mydas along the Queensland Coast, Australia. Journal of Aquatic Animal Health. 2017;29(3):150–7. doi: 10.1080/08997659.2017.1330783 28524816
29. Greenblatt RJ, Balazs GH, Casey JW, Work TM, Dutton P, Sutton CA, et al. Geographic variation in marine turtle fibropapillomatosis. Journal of Zoo and Wildlife Medicine. 2005;36(3):527–30. doi: 10.1638/04-051.1 17312778
30. Reich KJ, Bjorndal KA, Bolten AB. The ‘lost years’ of green turtles: using stable isotopes to study cryptic lifestages. Biology Letters. 2007;3(6):712–4. doi: 10.1098/rsbl.2007.0394 17878144
31. Anderson JD, Shaver DJ, Karel WJ. Genetic Diversity and Natal Origins of Green Turtles (Chelonia mydas) in the Western Gulf of Mexico. Journal of Herpetology. 2013;47(2):251–7. doi: 10.1670/12-031
32. Dutton PH, Jensen MP, Frutchey K, Frey A, LaCasella E, Balazs GH, et al. Genetic Stock Structure of Green Turtle (Chelonia mydas) Nesting Populations Across the Pacific Islands. Pacific Science. 2014;68(4):451–64. doi: 10.2984/68.4.1
33. Lahanas PN, Bjorndal KA, Bolten AB, Encalada SE, Miyamoto MM, Valverde RA, et al. Genetic composition of a green turtle (Chelonia mydas) feeding ground population: evidence for multiple origins. Marine Biology. 1998;130(3):345–52. doi: 10.1007/s002270050254
34. Musick JA, Limpus C. Habitat utilization and migration in juvenile sea turtles. In: Lutz PL, Musick JA, editors. The biology of sea turtles. 1. United States of America: CRC Press; 1997. p. 137–63.
35. Limpus CJ. A biological review of Australian marine turtle species. 2. Green turtle, Chelonia mydas (Linnaeus). Queensland, Australia: Queensland Environmental Protection Agency, 2008.
36. Chaloupka M, Bjorndal KA, Balazs GH, Bolten AB, Ehrhart LM, Limpus CJ, et al. Encouraging outlook for recovery of a once severely exploited marine megaherbivore. Global Ecology and Biogeography. 2008;17(2):297–304. doi: 10.1111/j.1466-8238.2007.00367.x
37. Dobbs K. MARINE TURTLES in the Great Barrier Reef World Heritage Area. Queensland: 2001.
38. Gulko D, and Eckert K. Sea turtles: An Ecological Guide. Hawaii: Mutual Publishing; 2004.
39. Hargrove S, Work T, Brunson S, Foley AM, Balazs G. Proceedings of the 2015 international summit on fibropapillomatosis: global status, trends, and population impacts. NOAA Technical Memorandum. 2016;NOAA-TM-NMFS-PIFSC-54,:87.
40. Limpus CJ, Reed PC. The green turtle, Chelonia mydas, in Queensland, a preliminary description of the population structure in a coral reef feeding ground. In: Grigg GC, Shine R, Ehmann H, editors. Biology of Australasian frogs and reptiles. Chipping Norton, N.S.W: Surrey Beatty in association with The Royal Zoological Society of New South Wales; 1985. p. 47–52.
41. Limpus CJ, Couper PJ, Read MA. The loggerhead turtle, Caretta caretta, in Queensland: Population structure in a warm temperate feeding area. Memoirs of the Queensland Museum Brisbane. 1994;37(1):195–204.
42. Limpus CJ. The hawksbill turtle, Eretmochelys imbricata, in Queensland: population structure within a southern Great Barrier Reef feeding ground. Wildlife Research. 1992;19(4):489–505. doi: 10.1071/WR9920489
43. Limpus CJ, Couper PJ, Read MA. The green turtle, Chelonia mydas, in Queensland: Population structure in a warm temperature feeding area. Memoirs of the Queensland Museum Brisbane. 1994;35(1):139–54.
44. Lu Y, Yu Q, Zamzow JP, Wang Y, Losey GS, Balazs GH, et al. Detection of Green Turtle Herpesviral Sequence in Saddleback WrasseThalassoma duperrey: A Possible Mode of Transmission of Green Turtle Fibropapilloma. Journal of Aquatic Animal Health. 2000;12(1):58–63. doi: 10.1577/1548-8667(2000)012<0058:DOGTHS>2.0.CO;2 28880781
45. Monezi TA, Mehnert DU, de Moura EMM, Müller NMG, Garrafa P, Matushima ER, et al. Chelonid herpesvirus 5 in secretions and tumor tissues from green turtles (Chelonia mydas) from Southeastern Brazil: A ten-year study. Veterinary microbiology. 2016;186:150–6. doi: 10.1016/j.vetmic.2016.02.020 27016769
46. Origgi FC, Tecilla M, Pilo P, Aloisio F, Otten P, Aguilar-Bultet L, et al. A Genomic Approach to Unravel Host-Pathogen Interaction in Chelonians: The Example of Testudinid Herpesvirus 3. PLoS One. 2015;10(8):e0134897. Epub 2015/08/06. doi: 10.1371/journal.pone.0134897 26244892.
47. Bender FC, Samanta M, Heldwein EE, Manuel Ponce de L, Bilman E, Lou H, et al. Antigenic and Mutational Analyses of Herpes Simplex Virus Glycoprotein B Reveal Four Functional Regions. Journal of Virology. 2007;81(8):3827–41. doi: 10.1128/JVI.02710-06 17267495
48. Coberley SS, Condit RC, Herbst LH, Klein PA. Identification and Expression of Immunogenic Proteins of a Disease-Associated Marine Turtle Herpesvirus. Journal of Virology. 2002;76(20):10553–8. doi: 10.1128/JVI.76.20.10553-10558.2002 12239336
49. Ackermann M, Leong J-AC, Koriabine M, Hartmann-Fritsch F, de Jong PJ, Lewis TD, et al. The genome of Chelonid herpesvirus 5 harbors atypical genes. Public Library of Science. 2012;7(10):e46623.
50. Jones K, Jensen M, Burgess G, Leonhardt J, van Herwerden L, Hazel J, et al. Closing the gap: Mixed stock analysis of three foraging populations of green turtles (Chelonia mydas) on the Great Barrier Reef. PeerJ. 2018;6(e5651). https://doi.org/10.7717/peerj.5651.
51. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England). 2012;28(12):1647–9. Epub 2012/05/01. doi: 10.1093/bioinformatics/bts199 22543367.
52. Jensen MP, Bell I, Limpus CJ, Hamann M, Ambar S, Whap T, et al. Spatial and temporal genetic variation among size classes of green turtles (Chelonia mydas) provides information on oceanic dispersal and population dynamics. Marine Ecology Progress Series. 2016;543:241–56.
53. Thompson JD, Thompson JD, Higgins DG, Higgins DG, Gibson TJ, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research. 1994;22(22):4673–80. doi: 10.1093/nar/22.22.4673 7984417
54. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. MOLECULAR BIOLOGY AND EVOLUTION. 2018;35(6):1547–9.
55. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of molecular evolution. 1980;16(2):111–20. doi: 10.1007/bf01731581 7463489
56. Jukes TH, Cantor CR. Evolution of protein molecules. In: Munro HN, editor. Mammalian Protein Metabolism. New Yo: Academic Press; 1969. p. 21–132.
57. Morrison CL, Iwanowici L, Work TM, Fahsbender E, Breitbart M, Adams C, et al. Genomic evolution, recombination, and inter-strain diversity of chelonid alphaherpesvirus 5 from Florida and Hawaii green sea turtles with fibropapillomatosis. PeerJ. 2018;6(2):e4386. doi: 10.7717/peerj.4386 29479497
58. Alfaro-Núñez A, Gilbert TP. Validation of a sensitive PCR assay for the detection of Chelonid fibropapilloma-associated herpesvirus in latent turtle infections. Journal of virological methods. 2014;206:38–41. doi: 10.1016/j.jviromet.2014.05.019 24882497
59. Ariel E, Lee K, Jones K, Scott J, Picard J. Arcobacter infection and temporary regression of tumours in a green turtle (Chelonia mydas) with fibropapillomatosis. Australian Veterinary Journal. 2017;Submitted.
60. Lawrance MF, Mansfield KL, Sutton E, Savage AE. Molecular evolution of fibropapilloma-associated herpesviruses infecting juvenile green and loggerhead sea turtles. Virology. 2018;521:190–7. doi: 10.1016/j.virol.2018.06.012 29960922
61. Mashkour N, Maclaine A, Burgess GW, Ariel E. Discovery of an Australian Chelonia mydas papillomavirus via green turtle primary cell culture and qPCR. Journal of Virological Methods. 2018;258:13–23. doi: 10.1016/j.jviromet.2018.04.004 29630942
62. Shimada T, Jones R, Limpus C, Groom R, Hamann M. Long-term and seasonal patterns of sea turtle home ranges in warm coastal foraging habitats: Implications for conservation. Marine Ecology Progress Series. 2016;562:163–79. doi: 10.3354/meps11972
63. Brown IH, Capua I, Cattoli G, Chen HL, Cox N, Davis CT, et al. Continuing progress towards a unified nomenclature for the highly pathogenic H5N1 avian influenza viruses: divergence of clade 2.2 viruses. INFLUENZA AND OTHER RESPIRATORY VIRUSES. 2009;3(2):59–62. doi: 10.1111/j.1750-2659.2009.00078.x 19496842
64. Donis RO, Smith GJD, Perdue ML, Brown IH, Chen H, Fouchier RAM, et al. Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerging Infectious Diseases. 2008;14(7):e1–e. doi: 10.3201/eid1407.071681 18598616
65. Smith GJD, Donis RO, Working WOFHNE, Group WOFHNEW. Continued evolution of highly pathogenic avian influenza A (H5N1): updated nomenclature. Influenza and Other Respiratory Viruses. 2012;6(1):1–5. doi: 10.1111/j.1750-2659.2011.00298.x 22035148
66. Diel DG, da Silva LHA, Liu H, Wang Z, Miller PJ, Afonso CL. Genetic diversity of avian paramyxovirus type 1: Proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes. Infection, Genetics and Evolution. 2012;12(8):1770–9. doi: 10.1016/j.meegid.2012.07.012 22892200
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