Archives of Virology

, Volume 155, Issue 8, pp 1261–1271 | Cite as

Comparative study of ranavirus isolates from cod (Gadus morhua) and turbot (Psetta maxima) with reference to other ranaviruses

  • Ellen Ariel
  • Riikka Holopainen
  • Niels Jørgen Olesen
  • Hannele Tapiovaara
Original Article

Abstract

Two iridovirus isolates recovered from cod (Gadus morhua) and turbot (Psetta maxima) in Denmark were examined in parallel with a panel of other ranaviruses including frog virus 3 (FV3), the reference strain for the genus Ranavirus. The isolates were assessed according to their reactivity in immunofluoresent antibody tests (IFAT) using both homologous and heterologous antisera and their amplification in PCR using primers targeting five genomic regions. The corresponding PCR fragments were sequenced, and the sequences obtained were used in phylogenetic analysis. In addition, the pathogenicity to rainbow trout under experimental challenge conditions was investigated. The viruses were serologically and genetically closely related to highly pathogenic ranaviruses such as European catfish iridovirus (ECV), European sheatfish iridovirus (ESV) and epizootic haematopoietic necrosis virus (EHNV). The challenge trials indicate that rainbow trout fry cultured at 15°C are not target species for the virus isolates in the present panel. We suggest that the two isolates belong in the genus Ranavirus and propose the name Ranavirus maxima (Rmax) for the turbot isolate.

Keywords

Rainbow Trout Major Capsid Protein Infectious Pancreatic Necrosis Virus Epithelioma Papulosum Cyprini Epithelioma Papulosum Cyprini Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The present work was partly funded by the 6th framework program of European Union contract number SSPE-CT-2005-006459, project RANA. Drs. Ahne, Bovo, Hyatt, de Kinkelin, Larsen, Nakajima, Owens and Whittington are acknowledged for providing iridovirus strains and antibodies. Thanks are due to all our technicians, but especially Nicole Nicolajsen.

Conflict of interest statement

The authors declare that they have no conflict of interest.

References

  1. 1.
    Chinchar VG, Essbauer S, He JG, Hyatt AD, Miyazaki T, Seligy V, Williams T (2005) Family Iridoviridae. In: Fauguet CM, Mayo MA, Maniloff J, desselberger U, Ball LA (eds) Virus Taxonomy. Eighth report of the International Committee on the taxonomy of Viruses. Elsevier Academic Press, London, pp 145–162Google Scholar
  2. 2.
    Goorha R (1982) Frog virus 3 DNA replication occurs in two stages. J Virol Aug 43(2):519–528Google Scholar
  3. 3.
    Jancovich JK, Davidson EW, Morado JF, Jacobs BL, Collins JP (1997) Isolation of a lethal virus from the endangered tiger salamander Ambystoma tigrinum stebbinsi. Dis Aquat Organ 31:161–167CrossRefGoogle Scholar
  4. 4.
    Zupanovic Z, Musso C, Lopez G, Louriero CL, Hyatt AD, Hengstberger S, Robinson AJ (1998) Isolation and characterization of iridoviruses from the giant toad Bufo marinus in Venezuela. Dis Aquat Organ 33:1–9CrossRefPubMedGoogle Scholar
  5. 5.
    Zhang QY, Xiao F, Li ZQ, Gui JF, Mao J, Chinchar VG (2001) Characterisation of an iridovirus from the cultured pig frog Rana grylio with lethal syndrome. Dis Aquat Organ 48:27–36CrossRefGoogle Scholar
  6. 6.
    Weng SP, He JG, Wang XH, Lu L, Deng M, Chan SM (2002) Outbreaks of an iridovirus disease in cultured tiger frog, Rana tigrina rugulosa, in southern China. J Fish Dis 25:423–427CrossRefGoogle Scholar
  7. 7.
    Westhouse RA, Jacobson ER, Harris RK, Winter KR, Homer BL (1996) Respiratory and pharyngoesophageal iridovirus infection in a gopher tortoise (Gopherus polyphemus). J Wildl Dis 32:682–686PubMedGoogle Scholar
  8. 8.
    Marschang RE, Becher P, Posthaus H, Wild P, Thiel HJ, Muller-Boblies U, Kaleta EF, Bacciarini LN (1999) Isolation and characterisation of an iridovirus from Hermann’s tortoise (Testudi hermanni). Arch Virol 144:1909–1922CrossRefPubMedGoogle Scholar
  9. 9.
    Chen ZX, Zheng JC, Jiang YL (1999) A new iridovirus isolated from soft-shelled turtle. Virus Res 63:147–151CrossRefPubMedGoogle Scholar
  10. 10.
    Just F, Essbauer S, Ahne W, Blahak S (2001) Occurrence of an Invertebrate Iridescent-like virus (Iridoviridae) in Reptiles. J Vet Med B48:685–694CrossRefGoogle Scholar
  11. 11.
    Drury SEN, Gough RE, Calvert I (2002) Detection and isolation of an iridovirus from chameleons (Chamaeleo quadricornis and Chamaeleo hoehnelli) in the United Kingdom. Vet Rec 150:451–452PubMedGoogle Scholar
  12. 12.
    Hyatt AD, Williamson M, Coupar BEH, Middleton D, Hengstberger SG, Gould AR, Selleck P, Wise TG, Kattenbelt J, Cunningham AA, Lee J (2002) First identification of a ranavirus from green pythons (Chondropython viridis). J Wildl Dis 38(2):239–252PubMedGoogle Scholar
  13. 13.
    Langdon JS, Humphrey JD, Williams LM, Hyatt AD, Westbury HA (1986) First virus isolation from Australian fish: an iridovirus-like pathogen from redfin perch, Perca fluviatilis L. J Fish Dis 9:263–268CrossRefGoogle Scholar
  14. 14.
    Langdon JS, Humphrey JD (1987) Epizootic haematopoietic necrosis, a new viral disease in redfin perch, Perca fluviatilis L., in Australia. J Fish Dis 10:289–297CrossRefGoogle Scholar
  15. 15.
    Langdon JS, Humphrey JD, Williams LM (1988) Outbreaks of an EHNV-like iridovirus in cultured rainbow trout, Salmo gairdneri Richardson, in Australia. J Fish Dis 11:93–96CrossRefGoogle Scholar
  16. 16.
    Ahne W, Schlotfeldt HJ, Thomsen I (1989) Fish viruses: Isolation of an icosahedral cytoplasmic deoxyribovirus from sheatfish (Siluris glanis). J Vet Med B 36:333–336CrossRefGoogle Scholar
  17. 17.
    Pozet F, Morand M, Moussa A, Torhy C, de Kinkelin P (1992) Isolation and preliminary characterisation of a pathogenic icosahedral deoxyribovirus from the catfish Ictalurus melas. Dis Aquat Organ 14:35–42CrossRefGoogle Scholar
  18. 18.
    Bovo G, Comuzi M, De Mas S, Ceschia G, Giorgetti G, Giacometti P, Cappellozza E (1993) Isolamento di un agente virale irido-like da pesce gatto (Ictalurus melas) dallevamento. Bollettino Societa Italiana di Patologia Ittica 11:3–10Google Scholar
  19. 19.
    Tapiovaara H, Olesen NJ, Lindén J, Rimaila-Pärnänen E, von Bonsdorff C-H (1998) Isolation and characterization of an irido-type virus from pike-perch (Stizostedion lucioperca). Dis Aquat Organ 32:185–193CrossRefPubMedGoogle Scholar
  20. 20.
    Bang Jensen B, Ersbøll AK, Ariel E (2009) Susceptibility of Pike Esox lucius to a panel of ranavirus isolates. Dis Aquat Org 83:169–179CrossRefGoogle Scholar
  21. 21.
    Granoff A, Came PE, Rafferty KA (1965) The isolation and properties of viruses from Rana pipiens: Their possible relationship to the renal adenocarcinoma of the leopard frog. Ann NY Acad Sci 126:237–255CrossRefPubMedGoogle Scholar
  22. 22.
    Speare R, Smith JR (1992) An iridovirus-like agent isolated from the borrowing frog, Lymnodynastes ornatus in northern Australia. Dis Aquat Org 14:51–57CrossRefGoogle Scholar
  23. 23.
    Cullen BR, Owens L (2002) Experimental challenge and clinical cases of Bohle irodovirus (BIV) in native Australian anurans. Dis Aquat Org 49:83–92CrossRefPubMedGoogle Scholar
  24. 24.
    Moody NJG, Owens L (1994) Experimantal demonstration of the pathogenicity of a frog virus, Bohle iridovirus, for a fish species, barramundi Lates calcarifer. Dis Aquat Organ 18:95–102CrossRefGoogle Scholar
  25. 25.
    Ariel E, Owens L (1997) Epizootic mortalities in tilapia (Oreochromis mossambicus). Dis Aquat Org 29:1–6CrossRefGoogle Scholar
  26. 26.
    Holopainen R, Ohlemeyer S, Schütze H, Bergmann SM, Tapiovaara H (2009) Ranavirus phylogeny and differentiation based on major capsid protein, DNA polymerase and neurofilament triplet H1-like protein genes. Dis Aquat Org 85:81–91CrossRefPubMedGoogle Scholar
  27. 27.
    Cunningham AA, Langton TES, Bennett PM, Lewin JF, Drury SEN, Gough RE, MacGregor SK (1996) Pathological and microbiological findings from incidents of unusual mortality of the common frog (Rana temporaria). Philos Trans R Soc Lond B 351:1539–1557CrossRefGoogle Scholar
  28. 28.
    Hoser R (1996) The frog decline in Australia. The reptilian magazine 4(3):19–25Google Scholar
  29. 29.
    Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R (1999) Emerging infectious diseases and amphibian population declines. Emerg Infect Dis 5(6):735–748CrossRefPubMedGoogle Scholar
  30. 30.
    Jensen NJ, Bloch B, Larsen JL (1979) A preliminary virological report. Nordisk Veterinaer 31:436–442Google Scholar
  31. 31.
    Bloch B, Larsen JL (1993) An iridovirus-like agent associated with systemic infection in cultured turbot Scophthalmus maximus fry in Denmark. Dis Aquat Organ 15:235–240CrossRefGoogle Scholar
  32. 32.
    Shi C-Y, Wang Y-G, Yang S-L, Huang J, Wang Q-Y (2004) The first report of an iridovirus-like agent infection in farmed turbot, Scophthalmus maximus, in China. Aquaculture 236:11–25CrossRefGoogle Scholar
  33. 33.
    Kim W-S, Oh M-J, Jung S-J, Kim Y-J, Kitamura S-I (2005) Characterization of an iridovirus detected from cultured turbot Scophthalmus maximus in Korea. Dis Aquat Organ 64:175–180CrossRefPubMedGoogle Scholar
  34. 34.
    Hedrick RP, McDowell TS, Ahne W, Torhy C, de Kinkelin P (1992) Properties of thre iridovirus-like agents associated with systemic infections of fish. Dis Aquat Organ 13:203–209CrossRefGoogle Scholar
  35. 35.
    Hengstberger SG, Hyatt A, Speare R, Coupar BEH (1993) Comparison of epizootic haematopoietic necrosis virus and Bohle iridovirus, recently isolated Australian iridoviruses. Dis Auqat Organ 15:93–107CrossRefGoogle Scholar
  36. 36.
    Ahne W, Bearzotti M, Bremont M, Essbauer S (1998) Comparison of European piscine and amphibian iridoviruses with epizootic haematopoietic necrosis virus and frog virus 3. J Med Vet B 45:373–383CrossRefGoogle Scholar
  37. 37.
    Hyatt AD, Gould AR, Zupanovic Z, Cunningham AA, Hengstberger S, Whittington RJ, Kattenbelt J, Coupar BEH (2000) Comparative studies of piscine and amphibian iridoviruses. Arch Virol 145:301–331CrossRefPubMedGoogle Scholar
  38. 38.
    Wolf K, Gravel M, Malsberger RG (1966) Lymphocystis virus:isolation in a centrarchid fish cell line. Science 151:1004–1005CrossRefPubMedGoogle Scholar
  39. 39.
    Frerichs GN, Rodger HD, Peric Z (1996) Cell culture isolation of piscine neuropathy nodavirus from juvenile sea bass Dicentrarchus labrax. J Gen Virol 77:2067–2071CrossRefPubMedGoogle Scholar
  40. 40.
    Reed LJ, Muench H (1938) A simple method of estimation of 50% endpoints. Am J Hyg 27:493–497Google Scholar
  41. 41.
    Olesen NJ, Lorenzen E, La Patra S (1999) Production of neutralizing antisera against viral haemorrhagic septicaemia (VHS) virus by intravenous injections of rabbits. J Aquat Anim Health 11:10–16CrossRefGoogle Scholar
  42. 42.
    Jørgensen PEV, Olesen NJ, Ahne W, Lorenzen N (1989) SVCV and PFR viruses: serological examination of 22 isolates indicates close relationship between the two fish rhabdoviruses. In: Ahne W, Kurstak E (eds) Viruses of lower vertebrates. Springer, Berlin, pp 349–366Google Scholar
  43. 43.
    Jørgensen PEV, Grauballe PC (1971) Problems in the serological typing of IPN virus. Acta Vet Scand 12:145–147Google Scholar
  44. 44.
    Koski P, Hill BJ, Way K, Neuvonen E, Rintamäki P (1992) A rhabdovirus isolated from brown trout (Salmo trutta m. lacustris [L]) with lesions in parenchymatous organs. Bull Eur Ass Fish Pathol 12(5):177–180Google Scholar
  45. 45.
    Björklund HV, Olesen NJ, Jørgensen PEV (1994) Biophysical and serological characterization of rhabdovirus 903/87 isolated from European lake trout Salmo trutta lacustris. Dis Aquat Org 19:21–26CrossRefGoogle Scholar
  46. 46.
    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multible sequence alignment aided by quality analysis tools. Nucleic Acid Res 25:4876–4882CrossRefPubMedGoogle Scholar
  47. 47.
    Nicholas KB, Nicholas HB Jr, Deerfield DW II (1997) GeneDoc: analysis and visualization of genetic variation, EMBNEW.NEWS 4:14Google Scholar
  48. 48.
    Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  49. 49.
    Lorenzen N, Olesen NJ, Jørgensen PEV (1993) Antibody response to VHS virus proteins in rainbow trout. Fish and Shellfish Immunol 3:461–473CrossRefGoogle Scholar
  50. 50.
    Anonymous (2001) Commission Decision of 22 February 2001. Laying down the sampling plans and diagnostic methods for the detection and confirmation of certain fish diseases and repealing Decision 92/532/EEC. 2001/183/EC. Off J Euro Commun L 067, 0065-0076.Google Scholar
  51. 51.
    Tan WG, Barkman TJ, Chinchar VG, Essani K (2004) Comparative genomic analyses of frog virus 3, type species of the genus Ranavirus (family Iridoviridae). Virology 323:70–84CrossRefPubMedGoogle Scholar
  52. 52.
    Pallister J, Gould A, Harrison D, Hyatt A, Jancovich J, Heine H (2007) Development of real-time PCR assays for the detection and differentiation of Australian and European ranaviruses. J Fish Dis 30:427–438CrossRefPubMedGoogle Scholar
  53. 53.
    Marsh IB, Whittington RJ, O′Rourke B, Hyatt AD, Chisholm O (2002) Rapid differentiation of Australian, European and American ranaviruses based on variation in major capsid protein gene sequence. Mol Cell Probes 16:137–151CrossRefPubMedGoogle Scholar
  54. 54.
    Mao J, Tham TN, Gentry GA, Aubertin A, Chinchar VG (1996) Cloning, sequence analysis, and expression of the major capsid protein of the iridovirus Frog virus 3. Virology 216:431–436CrossRefPubMedGoogle Scholar
  55. 55.
    Jancovich JK, Mao J, Chinchar VG, Wyatt C, Case ST, Kumar S, Valente G, Subramanian S, Davidson EW, Collins JP, Jacobs BL (2003) Genomic sequence of a ranavirus (family Iridoviridae) associated with salamander mortalities in North America. Virology 316:90–103CrossRefPubMedGoogle Scholar
  56. 56.
    He JG, Lü L, Deng M, He HH, Weng SP, Wang XH, Zhou SY, Long QX, Wang XZ, Chan SM (2002) Sequence analysis of the complete genome of an iridovirus isolated from the tiger frog. Virology 292:185–197CrossRefPubMedGoogle Scholar
  57. 57.
    Song WJ, Qin QW, Qiu J, Huang CH, Wang F, Hew CL (2004) Functional genomics analysis of Singapore Grouper Iridovirus: Complete sequence determination and proteomic analysis. J Virol 78:12576–12590CrossRefPubMedGoogle Scholar
  58. 58.
    Tsai CT, Ting JW, Wu MH, Wu MF, Guo IC, Chang CY (2005) Complete genome sequence of the grouper iridovirus and comparison of genomic organization with those of other iridoviruses. J Virol 79:2010–2023CrossRefPubMedGoogle Scholar
  59. 59.
    Mao J, Hedrick RP, Chinchar VG (1997) Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology 229:212–220CrossRefPubMedGoogle Scholar
  60. 60.
    Mao J, Gree DE, Fellers G, Chinchar VG (1999) Molecular characterization of iridoviruses isolated from sympatric amphibians and fish. Virus Res 63:45–52CrossRefPubMedGoogle Scholar
  61. 61.
    Mao J, Wang J, Chinchar GD, Chinchar VG (1999) Molecular characterization of a ranavirus isolated from largemouth bass Micropterus salmoides. Dis Aquat Org 37:107–114CrossRefPubMedGoogle Scholar
  62. 62.
    Bollinger TK, Mao J, Schock D, Brigham RM, Chinchar VG (1999) Pathology, isolation, and preliminary molecular characterization of a novel iridovirus from tiger salamanders in Saskatchewan. J Wildl Dis 35:413–429PubMedGoogle Scholar
  63. 63.
    Qin QW, Chang SF, Ngoh-Lim GH, Gibson Kueh S, Shi C, Lam TJ (2003) Characterization of a novel ranavirus isolated from grouper Epinephelus tauvina. Dis Aquat Org 53:1–9CrossRefPubMedGoogle Scholar
  64. 64.
    Greer AL, Berrill M, Wilson PJ (2005) Five Amphibian mortality events associated with ranavirus infection on south central Ontario, Canada. Dis Aquat Org 67:9–14CrossRefPubMedGoogle Scholar
  65. 65.
    Eaton HE, Metcalf J, Penny E, Tcherepanov V, Upton C, Brunetti CR (2007) Comparative genomic analysis of the family Iridoviridae: re-annotating and defining the core set of iridovirus genes. Virol J 4:11CrossRefPubMedGoogle Scholar
  66. 66.
    Huelsenbeck JP, Bull JJ, Cunningham CW (1996) Combining data in phylogenetic analysis. TREE 11:152–158Google Scholar
  67. 67.
    Whittington RJ, Reddacliff LA, Marsh I, Kearns C, Zupanovic Z, Callinan RC (1999) Further observations on the epidemiology and spread of epizootic haematopoietic necrosis virus (EHNV) in farmed rainbow trout Oncorhynchus mykiss in southeastern Australia and a recommended sampling strategy for surveillance. Dis Aquat Organ 35:125–130CrossRefPubMedGoogle Scholar
  68. 68.
    Le Morvan C, Troutaud D, Deschaux P (1998) Differential effects of temperature on specific and non-specific immune defences in fish. J Exp Biol 201:165–168PubMedGoogle Scholar
  69. 69.
    Whittington RJ, Reddacliff GL (1995) Influence of environmental temperature on experimental infection of redfin perch (Perca fluviatilis) and rainbow trout (Oncorhynchus mykiss) with epizootic haematopoietic necrosis virus—an Australian iridovirus. Aust Vet J 72:421–424CrossRefPubMedGoogle Scholar
  70. 70.
    Ahne W, Ogawa M, Schlotfeldt HJ (1990) Fish viruses: transmission and pathogenicity of an icosahedral cytoplasmic deoxyribovirus isolated from sheatfish (Silurus glanis). Zentralbl Veterinarmed B 37(3):187–190PubMedGoogle Scholar
  71. 71.
    Brunner JL, Richards K, Collins JP (2005) Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144:399–406CrossRefPubMedGoogle Scholar
  72. 72.
    Ariel E, Bang Jensen B (2009) Challenge studies of European stock of redfin perch, Perca fluviatilis L. and rainbow trout, Oncorhyncus mykiss (Wallbaum) with epizootic haematopoietic necrosis virus (EHNV). J Fish Dis 32:1017–1025. doi: 10.1111/j.1365-2761.2009.01088.x
  73. 73.
    Bang Jensen B, Ohlemeyer S, Holopainen R, Schuetze H, Tapiovaara H, Bergmann SM and Ariel E. Susceptibility of European farmed freshwater fish to a panel of ranaviruses. (Accepted Journal of Fish Diseases)Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Ellen Ariel
    • 1
    • 3
  • Riikka Holopainen
    • 2
  • Niels Jørgen Olesen
    • 1
  • Hannele Tapiovaara
    • 2
  1. 1.National Veterinary InstituteTechnical University of DenmarkÅrhusDenmark
  2. 2.Department of Veterinary VirologyFinnish Food Safety Authority EviraHelsinkiFinland
  3. 3.School of Veterinary and Biomedical SciencesJames Cook UniversityTownsvilleAustralia

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