Advertisement

Marine Biology

, Volume 162, Issue 1, pp 181–192 | Cite as

Phylogeographical analyses of shellfish viruses: inferring a geographical origin for ostreid herpesviruses OsHV-1 (Malacoherpesviridae)

  • Frédéric MineurEmail author
  • Jim Provan
  • Gareth Arnott
Original Paper

Abstract

Mortality episodes have regularly been affecting the shellfish industry throughout its history. Some of these mortalities, especially in the oyster industry, have been attributed to herpesviruses. Purification of viral particles and molecular characterization have led to the development of routine monitoring, as well as improved taxonomic classification. Ostreid herpesviruses (Malacoherpesviridae), mostly affecting Pacific oysters Crassostrea gigas, have been sporadically recorded in the French oyster industry since the early 1990s (OsHV-1 ‘reference’). From 2008, a new variant of ostreid herpesvirus (OsHV-1 μVar) has emerged and seriously impacted oyster production in France and other European countries. Consequently, the presence of ostreid herpesviruses has been monitored in different oyster producing areas around the world. The present study compiles molecular data that are available from survey efforts and takes a biogeographical approach, in order to infer an origin for ostreid herpesviruses. The highest genotype diversity was found in East Asia, despite a lower survey effort in that area than in Europe. Genotype network analyses show that both populations of ostreid herpesviruses present in Europe (OsHV-1 ‘reference’ and OsHV-1 μVar) are closely related to genotypes recorded in Asia. Moreover, ostreid herpesviruses have been detected in wild and symptom-free populations of various Asian native Crassostrea species. In the rest of the world, ostreid herpesvirus genotypes were recorded from cultivated C. gigas, and mostly associated with mortality episodes. Results of this study are therefore highly suggestive of an Asian origin for these viruses, which can be pathogenic under farming conditions. It also highlights the risks of European stock improvements, by means of overseas shellfish imports.

Keywords

Survey Effort Microsatellite Region Genotype Network European Genotype Oyster Production 
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.

Supplementary material

227_2014_2566_MOESM1_ESM.pdf (50 kb)
Supplementary material 1 (PDF 49 kb)

References

  1. AHAW (EFSA Panel on Animal Health and Welfare) (2010) Scientific opinion on the increased mortality events in Pacific oyster (Crassostrea gigas). EFSA J 8:1894Google Scholar
  2. Arzul I, Nicolas JL, Davison AJ, Renault T (2001a) French scallops: a new host for ostreid herpesvirus-1. Virology 290:342–349CrossRefGoogle Scholar
  3. Arzul I, Renault T, Lipart C, Davison AJ (2001b) Evidence for interspecies transmission of oyster herpesvirus in marine bivalves. J Gen Virol 82:865–870Google Scholar
  4. Batista FM, Taris N, Boudry P, Renault T (2005) Detection of ostreid herpesvirus-1 (OsHV-1) by PCR using a rapid and simple method of DNA extraction from oyster larvae. Dis Aquat Organ 64:1–4CrossRefGoogle Scholar
  5. Batista FM, Leitao A, Huvet A, Lapègue S, Heurtebise S, Boudry P (2009) The taxonomic status and origin of the Portuguese oyster Crassostrea angulata (Lamarck, 1819). Oyster Res Inst News 24:5–13Google Scholar
  6. Berthe FCJ, Choi KS, Figueras A, Soudant P, Villalba A (2004a) Perkinsosis in Europe: current issues and research needs. Bull Eur Assoc Fish Pathol 24:52–53Google Scholar
  7. Berthe FCJ, Le Roux F, Adlard RD, Figueras A (2004b) Marteiliosis in molluscs: a review. Aquat Living Resour 17:433–448CrossRefGoogle Scholar
  8. Berthelin C, Kellner K, Mathieu M (2000) Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (West Coast of France). Comp Biochem Phys B 125:359–369CrossRefGoogle Scholar
  9. Buestel D, Ropert M, Prou J, Goulletquer P (2009) History, status, and future of oyster culture in France. J Shellfish Res 28:813–820CrossRefGoogle Scholar
  10. Burge CA, Strenge RE, Friedman CS (2011) Detection of the oyster herpesvirus in commercial bivalve in northern California, USA: conventional and quantitative PCR. Dis Aquat Organ 94:107–116CrossRefGoogle Scholar
  11. Comps M, Cochennec N (1993) A herpes-like virus from the European oyster Ostrea edulis L. J Invertebr Pathol 62:201–203CrossRefGoogle Scholar
  12. Comps M, Duthoit JL (1976) Infection virale associée à la “maladie des branchies” de l’huître portugaise Crassostrea angulata LmK. Comptes Rendus de l’Académie des Sciences, Série D 283:1595–1597Google Scholar
  13. Comps M, Duthoit JL (1979) Infections virales chez les huîtres Crassostrea angulata Lmk. et Crassostrea gigas Thunberg. Haliotis 8:301–307Google Scholar
  14. Comps M, Bonami JR, Constantin V (1976) Une virose de l’huître portugaise (Crassostrea angulata LMK). Comptes Rendus de l’Académie des Sciences, Série D 282:139–143Google Scholar
  15. da Silva PM, Fuentes J, Villalba A (2005) Growth, mortality and disease susceptibility of oyster Ostrea edulis families obtained from brood stocks of different geographical origins, through on growing in the Ria de Arousa (Galicia, NW Spain). Mar Biol 147:965–977CrossRefGoogle Scholar
  16. Davison AJ, Trus BL, Cheng NQ, Steven AC, Watson MS, Cunningham C, Le Deuff RM, Renault T (2005) A novel class of herpesvirus with bivalve hosts. J Gen Virol 86:41–53CrossRefGoogle Scholar
  17. Davison AJ, Eberle R, Ehlers B, Hayward GS, McGeoch DJ, Minson AC, Pellett PE, Roizman B, Studdert MJ, Thiry E (2009) The order Herpesvirales. Arch Virol 154:171–177CrossRefGoogle Scholar
  18. Degremont L, Soletchnik P, Boudry P (2010) Summer mortality of selected juvenile Pacific oyster Crassostrea Gigas under laboratory conditions and in comparison with field performance. J Shellfish Res 29:847–856CrossRefGoogle Scholar
  19. Dundon WG, Arzul I, Omnes E, Robert M, Magnabosco C, Zambon M, Gennari L, Toffan A, Terregino C, Capua I, Arcangeli G (2011) Detection of Type 1 Ostreid Herpes variant (OsHV-1 μVar) with no associated mortality in French-origin Pacific cupped oyster Crassostrea gigas farmed in Italy. Aquaculture 314:49–52CrossRefGoogle Scholar
  20. EC (2010) Commission Regulation (EU) No 175/210 of 2 March 2010 implementing Council Directive 2006/88/EC as regards measures to control increase mortality in oysters of the species Crassostrea gigas in connection with the detection of Ostreid herpesvirus 1 µvar (OsHV-1 µvar). Off J Eur Union L52:1–13Google Scholar
  21. Farley CA (1978) Viruses and virus-like lesions in marine mollusks. Mar Fish Rev 40:18–20Google Scholar
  22. Farley CA, Foster WS, Banfield WG, Kasnic G (1972) Oyster herpes-type virus. Science 178:759–760CrossRefGoogle Scholar
  23. Friedman CS, Estes RM, Stokes NA, Burge CA, Hargove JS, Barber BJ, Elston RA, Burreson EM, Reece KS (2005) Herpes virus in juvenile Pacific oysters Crassostrea gigas from Tomales Bay, California, coincides with summer mortality episodes. Dis Aquat Organ 63:33–41CrossRefGoogle Scholar
  24. Garcia C, Thébault A, Dégremont L, Arzul I, Miossec L, Robert M, Chollet B, Francois C, Joly JP, Ferrand S, Kerdudou N, Renault T (2011) Ostreid herpesvirus 1 detection and relationship with Crassostrea gigas spat mortality in France between 1998 and 2006. Vet Res 42:73CrossRefGoogle Scholar
  25. Goulevant C (2004) L’Opération Résur http://www.portseudre.com/operation_resur.pdf. Accessed May 2014
  26. Grijalva-Chon JM, Castro-Longoria R, Ramos-Paredes J, Enriquez-Espinoza TL, Mendoza-Cano F (2013) Detection of a new OsHV-1 DNA strain in the healthy Pacific oyster, Crassostrea gigas Thunberg, from the Gulf of California. J Fish Dis 36:965–968Google Scholar
  27. Grizel H, Héral M (1991) Introduction into France of the Japanese oyster (Crassostrea gigas). Journal du Conseil International pour l’Exploration de la Mer 47:399–403CrossRefGoogle Scholar
  28. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  29. Hine PM, Thorne T (1997) Replication of herpes like viruses in haemocytes of adult flat oysters Ostrea angasi: an ultrastructural study. Dis Aquat Organ 29:189–196CrossRefGoogle Scholar
  30. Hine PM, Wesney B, Hay BE (1992) Herpesviruses associated with mortalities among hatchery-reared larval Pacific oysters Crassostrea gigas. Dis Aquat Organ 12:135–142CrossRefGoogle Scholar
  31. Hwang JY, Park JJ, Yu HJ, Hur YB, Arzul I, Couraleau Y, Park MA (2013) Ostreid herpesvirus 1 infection in farmed Pacific oyster larvae Crassostrea gigas (Thunberg) in Korea. J Fish Dis 36:969–972Google Scholar
  32. Jenkins C, Hick P, Gabor M, Spiers Z, Fell SA, Gu XN, Read A, Go J, Dove M, O’Connor W, Kirkland PD, Frances J (2013) Identification and characterisation of an ostreid herpesvirus-1 microvariant (OsHV-1 mu-var) in Crassostrea gigas (Pacific oysters) in Australia. Dis Aquat Organ 105:109–126CrossRefGoogle Scholar
  33. Jouaux A, Lafont M, Blin JL, Houssin M, Mathieu M, Lelong C (2013) Physiological change under OsHV-1 contamination in Pacific oyster Crassostrea gigas through massive mortality events on fields. BMC Genom 14:590CrossRefGoogle Scholar
  34. Lafferty KD, Porter JW, Ford SE (2004) Are diseases increasing in the ocean? Annu Rev Ecol Evol S 35:31–54CrossRefGoogle Scholar
  35. Le Deuff RM, Renault T (1999) Purification and partial genome characterization of a herpes-like virus infecting the Japanese oyster, Crassostrea gigas. J Gen Virol 80:1317–1322Google Scholar
  36. Lenihan HS, Micheli F, Shelton SW, Peterson CH (1999) The influence of multiple environmental stressors on susceptibility to parasites: an experimental determination with oysters. Limnol Oceanogr 44:910–924CrossRefGoogle Scholar
  37. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  38. Lynch SA, Carlsson J, Reilly AO, Cotter E, Culloty SC (2012) A previously undescribed ostreid herpes virus 1 (OsHV-1) genotype detected in the pacific oyster, Crassostrea gigas, in Ireland. Parasitology 139:1526–1532CrossRefGoogle Scholar
  39. Martenot C, Fourour S, Oden E, Jouaux A, Travaillé E, Malas JP, Houssin M (2012) Detection of the OsHV-1 µVar in the Pacific oyster Crassostrea gigas before 2008 in France and description of two new microvariants of the Ostreid Herpesvirus 1 (OsHV-1). Aquaculture 338:293–296CrossRefGoogle Scholar
  40. Martenot C, Travaillé E, Lethuillier O, Lelong C, Houssin M (2013) Genome exploration of six variants of the Ostreid Herpesvirus 1 and characterization of large deletion in OsHV-1 µVar specimens. Virus Res 178:462–470CrossRefGoogle Scholar
  41. Matthiessen GC (2001) Oyster culture. Fishing news books series. Wiley, London, p 162Google Scholar
  42. Mineur F, De Clerck O, Le Roux A, Maggs CA, Verlaque M (2010) Polyopes lancifolius (Halymeniales, Rhdophyta), a new component of the Japanese marine flora introduced to Europe. Phycologia 49:86–96CrossRefGoogle Scholar
  43. Mineur F, Le Roux A, Stegenga H, Verlaque M, Maggs CA (2012) Four new exotic red seaweeds on European shores. Biol Invasions 14:1635–1641CrossRefGoogle Scholar
  44. Mineur F, Le Roux A, Maggs CA, Verlaque M (2014) Positive feedback loop between introductions of non-indigenous marine species and cultivation of oysters in Europe. Conserv Biol. doi: 10.1111/cobi.12363
  45. Minson AC, Davison A, Eberle R, Desrosiers RC, Fleckenstein B, McGeoch DJ, Pellet PE, Roizman B, Studdert DMJ (2000) Family Herpesviridae. In: van Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB (eds) Virus taxonomy seventh report of the international committee on taxonomy of viruses. Academic Press, San Diego, pp 203–225Google Scholar
  46. Moss JA, Burreson EM, Cordes JF, Dungan CF, Brown GD, Wang A, Wu X, Reece KS (2007) Pathogens in Crassostrea ariakensis and other Asian oyster species: implications for non-native oyster introduction to Chesapeake Bay. Dis Aquat Organ 77:207–223CrossRefGoogle Scholar
  47. MPI (2010) Range of factors at play in oyster deaths. 8 December 2010. Biosecurity in New Zealand News. Internet communication. Ministry for Primary Industries of New Zealand. http://www.biosecurity.govt.nz/media/08-12-2010/range-of-factors-at-play-in-oyster-deaths. Accessed May 2014
  48. Nicolas JL, Comps M, Cochennec N (1992) Herpes-like virus infecting Pacific oyster larvae, Crassostrea gigas. Bull Eur Assoc Fish Pathol 12:11–13Google Scholar
  49. O Foighil D, Gaffney PM, Wilbur AE, Hilbish TJ (1998) Mitochondrial cytochrome oxidase I gene sequences support an Asian origin for the Portuguese oyster Crassostrea angulata. Mar Biol 131:497–503CrossRefGoogle Scholar
  50. Paillard C, Le Roux F, Borreg JJ (2004) Bacterial disease in marine bivalves, a review of recent studies: trends and evolution. Aquat Living Resour 17:477–498CrossRefGoogle Scholar
  51. Pernet F, Barret J, Le Gall P, Corporeau C, Degremont L, Lagarde F, Pepin JF, Keck N (2012) Mass mortalities of Pacific oysters Crassostrea gigas reflect infectious diseases and vary with farming practices in the Mediterranean Thau lagoon, France. Aquac Environ Interact 2:215–237CrossRefGoogle Scholar
  52. Petton B, Pernet F, Robert R, Boudry P (2013) Temperature influence on pathogen transmission and subsequent mortalities in juvenile Pacific oysters Crassostrea gigas. Aquac Environ Interact 3:257–273CrossRefGoogle Scholar
  53. Reece KS, Cordes JF, Stubbs JB, Hudson KL, Francis EA (2008) Molecular phylogenies help resolve taxonomic confusion with Asian Crassostrea oyster species. Mar Biol 153:709–721CrossRefGoogle Scholar
  54. Regoes RR, Hamblin S, Tanaka MM (2013) Viral mutation rates: modelling the roles of within-host viral dynamics and the trade-off between replication fidelity and speed. Proc R Soc B 280:20122047CrossRefGoogle Scholar
  55. Ren WC, Chen HX, Renault T, Cai YY, Bai CM, Wang CM, Huang J (2013) Complete genome sequence of acute viral necrosis virus associated with massive mortality outbreaks in the Chinese scallop, Chlamys farreri. Virol J 10:110CrossRefGoogle Scholar
  56. Renault T (2008) Shellfish viruses. In: Mahy BWJ, Van Regenmortel MHV (eds) Encyclopedia of virology, 3rd edn. Elsevier, Amsterdam, pp 560–567CrossRefGoogle Scholar
  57. Renault T (2011) Viruses infecting marine molluscs: increased mortality outbreaks and herpes viruses. B Acad Vet France 164:359–364CrossRefGoogle Scholar
  58. Renault T, Novoa B (2004) Viruses infecting bivalve molluscs. Aquat Living Resour 17:397–409CrossRefGoogle Scholar
  59. Renault T, Le Deuff RM, Cochennec N, Chollet B, Maffart P (1993) Contribution à l’étude de mollusques marins: Iridovirus-like et Herpèsvirus-like. Description, caractérisation biochimique, cycle de multiplication viral, diagnostic et étude épidémiologique. http://archimer.ifremer.fr/doc/00041/15230/
  60. Renault T, Le Deuff RM, Cochennec N, Maffart P (1994) Herpesviruses associated with mortalities among Pacific Oyster, Crassostrea gigas, in France: comparative study. Rev Med Vet-Toulouse 145:735–742Google Scholar
  61. Renault T, Le Deuff RM, Chollet B, Cochennec N, Gerard A (2000a) Concomitant herpes-like virus infections in hatchery-reared larvae and nursery-cultured spat Crassostrea gigas and Ostrea edulis. Dis Aquat Organ 42:173–183CrossRefGoogle Scholar
  62. Renault T, Le Deuff RM, Lipart C, Delsert C (2000b) Development of a PCR procedure for the detection of a herpes-like virus infecting oysters in France. J Virol Methods 88:41–50CrossRefGoogle Scholar
  63. Renault T, Lipart C, Arzul I (2001) A herpes-like virus infecting Crassostrea gigas and Ruditapes philippinarum larvae in France. J Fish Dis 24:369–376CrossRefGoogle Scholar
  64. Renault T, Moreau P, Faury N, Pepin JF, Segarra A, Webb S (2012) Analysis of clinical Ostreid Herpesvirus 1 (Malacoherpesviridae) specimens by sequencing amplified fragments from three virus genome areas. J Virol 86:5942–5947CrossRefGoogle Scholar
  65. Renault T, Tchaleu G, Faury N, Moreau P, Segarra A, Barbosa-Solomieu V, Lapegue S (2014) Genotyping of a microsatellite locus to differentiate clinical Ostreid herpesvirus 1 specimens. Vet Res 45:3CrossRefGoogle Scholar
  66. Roque A, Carrasco N, Andree KB, Lacuesta B, Elandaloussi L, Gairin I, Rodgers CJ, Furones MD (2012) First report of OsHV-1 microvar in Pacific oyster (Crassostrea gigas) cultured in Spain. Aquaculture 324–325:303–306CrossRefGoogle Scholar
  67. Ruesink JL, Lenihan HS, Trimble AC, Heiman KW, Micheli F, Byers JE, Kay MC (2005) Introduction of non-native oysters: ecosystem effects and restoration implications. Annu Rev Ecol Evol S 36:643–689CrossRefGoogle Scholar
  68. Samain JF, Dégremont L, Soletchnik P, Haure J, Bédier E, Ropert M, Moal J, Huvet A, Bacca H, Van Wormhoudt A, Delaporte M, Costil K, Pouvreau S, Lambert C, Boulo V, Soudant P, Nicolas JL, Le Roux F, Renault T, Gagnaire B, Geret F, Boutet I, Burgeot T, Boudry P (2007) Genetically based resistance to summer mortality in the Pacific oyster (Crassostrea gigas) and its relationship with physiological, immunological characteristics and infection processes. Aquaculture 268:227–243CrossRefGoogle Scholar
  69. Segarra A, Pépin JF, Arzul I, Morga B, Faury N, Renault T (2010) Detection and description of a particular Ostreid herpesvirus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Res 153:92–99CrossRefGoogle Scholar
  70. Shimahara Y, Kurita J, Kiryu I, Nishioka T, Yuasa K, Kawana M, Kamaishi T, Oseko N (2012) Surveillance of Type 1 Ostreid Herpesvirus (OsHV-1) variants in Japan. Fish Pathol 47:129–136CrossRefGoogle Scholar
  71. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583CrossRefGoogle Scholar
  72. Tang BJ, Liu BZ, Wang XM, Yue X, Xiang JH (2010) Physiological and immune responses of Zhikong scallop Chlamys farreri to the acute viral necrobiotic virus infection. Fish Shellfish Immunol 29:42–48CrossRefGoogle Scholar
  73. Wilber DH, Clarke DG (2001) Biological effects of suspended sediments: a review of suspended sediment impacts on fish and shellfish with relation to dredging activities in estuaries. N Am J Fish Manage 21:855–875CrossRefGoogle Scholar
  74. Wu X, Xiao S, Yu Z (2013) Mitochondrial DNA and morphological identification of Crassostrea zhanjiangensis sp. nov. (Bivalvia: Ostreidae): a new species in Zhanjiang, China. Aquat Living Resour 26:273–280CrossRefGoogle Scholar
  75. Xiangyun W, Xiaodong X, Ziniu Y, Zhenpeng W, Jianjun X (2010) Comparison of seven Crassostrea mitogenomes and phylogenetic analyses. Mol Phylogenet Evol 57:448–454CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.School of Biological Sciences/Institute for Global Food SecurityQueen’s University of BelfastBelfastUK
  2. 2.Phycology Research GroupGhent UniversityGhentBelgium

Personalised recommendations