Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T18:49:02.210Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of the mussel Mytilus spp. in the transmission of ostreid herpesvirus-1 microVar

Published online by Cambridge University Press:  21 December 2017

A. J. O’ Reilly ,
C. Laide ,
A Maloy ,
S. Hutton ,
B. Bookelaar ,
K. O’ Sullivan ,
S. A. Lynch  and
S. C. Culloty
A. J. O’ Reilly
Affiliation:
Aquaculture and Fisheries Development Centre, School of Biological, Earth and Environmental Sciences, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland Environmental Research Institute, University College Cork, Lee Rd., Cork, Ireland
C. Laide
Affiliation:
Aquaculture and Fisheries Development Centre, School of Biological, Earth and Environmental Sciences, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland
A Maloy
Affiliation:
U.S. Fish & Wildlife Service, Northeast Fishery Centre, PO Box 75, 227 Washington Ave Lamar PA, 16848, USA
S. Hutton
Affiliation:
Aquaculture and Fisheries Development Centre, School of Biological, Earth and Environmental Sciences, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland Environmental Research Institute, University College Cork, Lee Rd., Cork, Ireland
B. Bookelaar
Affiliation:
Aquaculture and Fisheries Development Centre, School of Biological, Earth and Environmental Sciences, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland Environmental Research Institute, University College Cork, Lee Rd., Cork, Ireland
K. O’ Sullivan
Affiliation:
School of Mathematical Sciences, Room 1.58, Western Gateway Building, University College Cork, Cork, Ireland
S. A. Lynch*
Affiliation:
Aquaculture and Fisheries Development Centre, School of Biological, Earth and Environmental Sciences, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland Environmental Research Institute, University College Cork, Lee Rd., Cork, Ireland
S. C. Culloty
Affiliation:
Aquaculture and Fisheries Development Centre, School of Biological, Earth and Environmental Sciences, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland Environmental Research Institute, University College Cork, Lee Rd., Cork, Ireland
*
Author for correspondence: S. A. Lynch, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The Pacific oyster Crassostrea gigas contributes significantly to global aquaculture; however, C. gigas culture has been affected by ostreid herpesvirus-1 (OsHV-1) and variants. The dynamics of how the virus maintains itself at culture sites is unclear and the role of carriers, reservoirs or hosts is unknown. Both wild and cultured mussels Mytilus spp. (Mytilus edulis, Mytilus galloprovincialis and hybrids) are commonly found at C. gigas culture sites. The objective of this study was to investigate if Mytilus spp. can harbour the virus and if viral transmission can occur between mussels and oysters. Mytilus spp. living at oyster trestles, 400–500 m higher up the shore from the trestles and up to 26 km at non-culture sites were screened for OsHV-1 and variants by all the World Organization for Animal Health (OIE) recommended diagnostic methods including polymerase chain reaction (PCR), quantitative PCR (qPCR), histology, in situ hybridization and confirmation using direct sequencing. The particular primers that target OsHV-1 and variants, including OsHV-1 microVar (μVar), were used in the PCR and qPCR. OsHV-1 μVar was detected in wild Mytilus spp. at C. gigas culture sites and more significantly the virus was detected in mussels at non-culture sites. Cohabitation of exposed wild mussels and naïve C. gigas resulted in viral transmission after 14 days, under an elevated temperature regime. These results indicate that mussels can harbour OsHV-1 μVar; however, the impact of OsHV-1 μVar on Mytilus spp. requires further investigation.

Keywords

CohabitationCrassostrea gigasHerpesvirusinterspecies transmissionMytilus spp.temperature
Type
Research Article
Information
Parasitology , Volume 145 , Issue 8 , July 2018 , pp. 1095 - 1104
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

References

Appolinário, C, Allendorf, SD, Vicente, AF, Ribeiro, BD, da Fonseca, CR, Antunes, JM, Peres, MG, Kotait, I, Carrieri, ML and Megid, J (2015) Fluorescent antibody test, quantitative polymerase chain reaction pattern and clinical aspects of rabies virus strains isolated from main reservoirs in Brazil. The Brazilian Journal of Infectious Diseases 19(5), 479–485.Google Scholar
Arzul, I, Nicolas, J-L, Davison, AJ and Renault, T (2001) French scallops: a new host for ostreid herpesvirus-1. Virology 290, 342–349.Google Scholar
Ashford, RW (2003) When is a reservoir not a reservoir? Emerging Infectious Diseases 9(11), 1495–1496.Google Scholar
Blankson, JN, Persaud, D and Siliciano, RF (2002) The challenge of viral reservoirs in HIV-1 infection. Annual Review of Medicine 53, 557–593.Google Scholar
Brachman, PS (1996). Epidemiology. In: Baron, S (ed.). Medical Microbiology, 4th edn. Galveston, TX: University of Texas Medical Branch at Galveston, Chapter 9. https://www.ncbi.nlm.nih.gov/books/NBK7993/Google Scholar
Burge, CA, Strenge, RE and Friedman, CS (2011) Detection of the oyster herpesvirus in commercial bivalves in northern California, USA: conventional and quantitative PCR. Diseases of Aquatic Organisms 94, 107–111.Google Scholar
Chang, PH, Kuo, ST, Lai, SH, Yang, HS, Ting, YY, Hsu, CL and Chen, HC (2005) Herpes-like virus infection causing mortality of cultured abalone Haliotis diversicolor supertexta in Taiwan. Diseases of Aquatic Organisms 65, 23–27.Google Scholar
Comps, M and Cochennec, N (1993) A herpes-like virus from the European oyster Ostrea edulis L. Journal of Invertebrate Pathology 62, 201–203.Google Scholar
Cotter, E, Malham, SK, O'Keeffe, S, Lynch, SA, Latchford, JW, King, JW, Beaumont, AR and Culloty, SC (2010) Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea: the influence of growth, biochemistry and gametogenesis. Aquaculture 303, 8–21.CrossRefGoogle Scholar
Dang, VY, Speck, P and Benkendorff, K (2012) Influence of elevated temperatures on the immune response of abalone, Haliotis rubra. Fish & Shellfish Immunology 32, 732–740.Google Scholar
Davison, AJ, Eberle, R, Ehlers, B, Hayward, GS, McGeoch, DJ, Minson, AC, Pellet, PE, Roizman, B, Studdert, MJ and Thiry, E (2009) The order Herpesvirales. Archives of Virology 154, 171–177.CrossRefGoogle ScholarPubMed
Domeneghetti, S, Varotto, L, Civettini, M, Rosani, U, Stauder, M, Pretto, T, Pezzati, E, Arcangeli, G, Turolla, E, Pallavicini, A and Venier, P (2014) Mortality occurrence and pathogen detection in Crassostrea gigas and Mytilus galloprovincialis close-growing in shallow waters (Goro lagoon, Italy). Fish & Shellfish Immunology 41, 37–44.Google Scholar
Dundon, WG, Arzul, I, Omnes, E, Robert, M, Magnabosco, C, Zambon, M, Gennari, L, Toffan, A, Terregino, C, Capua, I and 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, 49–52.Google Scholar
Ellis, RP, Widdicombe, S, Parry, H, Hutchinson, TH and Spicer, JI (2015) Pathogenic challenge reveals immune trade-off in mussels exposed to reduced seawater pH and increased temperature. Journal of Experimental Marine Biology and Ecology 462, 83–89.Google Scholar
Evans, O, Paul-Pont, I and Whittington, RJ (2017) Detection of ostreid herpesvirus 1 microvariant DNA in aquatic invertebrate species, sediment and other samples collected from the Georges River estuary, New South Wales, Australia. Diseases of Aquatic Organisms 122(3), 247–255.Google Scholar
Garcia, C, Thébault, A, Dégremont, L, Arzul, I, Miossec, L, Robert, M, Chollet, B, François, C, Joly, J.-P, Ferrand, S, Kerdudou, N and Renault, T (2011) Ostreid herpesvirus 1 detection and relationship with Crassostrea gigas spat mortality in France between 1998 and 2006. Vetinary Research 42, 73.Google Scholar
Haydon, DT, Cleaveland, S, Taylor, LH and Laurenson, MK (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8(12), 1468–1473.Google Scholar
Hine, PM and Thorne, T (1997) Replication of herpes-like viruses in haemocytes of adult flat oysters Ostrea angasi: an ultrastructural study. Diseases of Aquatic Organisms 29, 189–196.Google Scholar
Hine, PM, Wesney, B and Besant, P (1998) Replication of a herpes-like virus in larvae of the flat oyster Tiostrea chilensisat ambient temperatures. Diseases of Aquatic Organisms 32, 161–171.Google Scholar
Hu, M, Li, L, Sui, Y, Li, J, Wang, Y, Lu, W and Dupont, S (2015) Effect of pH and temperature on antioxidant responses of the thick shell mussel Mytilus coruscus. Fish & Shellfish Immunology 46, 573–583.Google Scholar
Jenkins, C, Hick, P, Gabor, M, Spiers, Z, Fell, SA, Gu, X, Read, A, Go, J, Dove, M, O’ Connor, W, Kirkland, PD and Frances, J (2013) Identification and characterisation of an ostreid herpesvirus-1 microvariant (OsHV-1 μ-var) in Crassostrea gigas (Pacific oysters) in Australia. Diseases of Aquatic Organisms 105, 109–126.CrossRefGoogle ScholarPubMed
Lipart, C and Renault, T (2002) Herpes-like virus detection in infected Crassostrea gigas spat using DIG-labelled probes. Journal of Virological Methods 101, 1–10.Google Scholar
Lynch, SA, Armitage, DV, Coughlan, J, Mulcahy, MF and Culloty, SC (2007) Investigating the possible role of benthic macroinvertebrates and zooplankton in the life cycle of the haplosporidian Bonamia ostreae. Experimental Parasitology 115, 359–368.CrossRefGoogle ScholarPubMed
Lynch, SA, Abollo, E, Ramilo, A, Cao, A, Culloty, SC and Villalba, A (2010) Observations raise the question if the Pacific oyster, Crassostrea gigas, can act as either a carrier or a reservoir for Bonamia ostreae or Bonamia exitiosa. Parasitology 137, 1515–1526.Google Scholar
Lynch, SA, Carlsson, J, Reilly, AO, Cotter, E and Culloty, S (2012) A previously undescribed ostreid herpes virus 1 (OsHV-1) genotype detected in the pacific oyster, Crassostrea gigas, in Ireland. Parasitology 139, 1526–1532.CrossRefGoogle ScholarPubMed
Lynch, SA, Dillane, E, Carlsson, J and Culloty, SC (2013) Development and assessment of a sensitive and cost-effective polymerase chain reaction to detect ostreid herpesvirus 1 and variants. Journal of Shellfish Research 32(3), 657–664.Google Scholar
Lynch, SA, Morgan, E, Carlsson, J, Mackenzie, C, Wooton, EC, Rowley, AF, Malham, S and Culloty, SC (2014) The health status of mussels, Mytilus spp., in Ireland and Wales with the molecular identification of a previously undescribed haplosporidian. Journal of Invertebrate Pathology 118, 59–65.CrossRefGoogle ScholarPubMed
Malham, SK, Cotter, E, O'Keeffe, S, Lynch, S, Culloty, SC, King, JW, Latchford, JW and Beaumont, AR (2009) Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea: the influence of temperature and nutrients on health and survival. Aquaculture 287, 128–138.Google Scholar
Martenot, C, Denechère, L, Hubert, P, Metayer, L, Oden, E, Trancart, S, Travaillé, E and Houssin, M (2015) Virulence of ostreid herpesvirus 1 μVar in sea water at 16 °C and 25 °C. Aquaculture 439, 1–6.CrossRefGoogle Scholar
Morrissey, T, McCleary, S, Collins, E, Henshilwood, K and Cheslett, D (2015) An investigation of ostried herpes virus microvariants found in Crassostrea gigas oyster producing bays in Ireland. Aquaculture 442, 86–92.Google Scholar
Paredes, E, Bellas, J and Adams, SL (2013) Comparative cryopreservation study of trochophore larvae from two species of bivalves: Pacific oyster (Crassostrea gigas) and Blue mussel (Mytilus galloprovincialis). Cryobiology 67, 274–279.CrossRefGoogle ScholarPubMed
Peeler, EJ, Reese, RA, Cheslett, DL, Geoghegan, F, Power, A and Thrush, MA (2012) Investigation of mortality in Pacific oysters associated with ostreid herpesvirus-1Var in the Republic of Ireland in 2009. Preventive Veterinary Medicine 105, 136–143.CrossRefGoogle ScholarPubMed
Pépin, JF, Riou, A and Renault, T (2008) Rapid and sensitive detection of ostreid herpesvirus 1 in oyster samples by real-time PCR. Journal of Virological Methods 149, 269–276.CrossRefGoogle ScholarPubMed
Pernet, F, Barret, J, Marty, C, Moal, J, Le Gall, P and Boudry, P (2010) Environmental anomalies, energetic reserves and fatty acid modifications in oysters coincide with an exceptional mortality event. Marine Ecology Progress Series 401, 129–146.Google Scholar
Pernet, F, Barret, J, Gall, PL, Corporeau, C, Dégremont, L, Lagarde, F, Pépin, J-F and Keck, N (2012) Mass mortalities of Pacific oysters Crassostrea gigas reflect infectious diseases and vary with farming practices in the Thau lagoon. Aquaculture Environment Interactions 2, 215–237.CrossRefGoogle Scholar
Pernet, F, Tamayo, D and Petton, B (2015) Influence of low temperatures on the survival of the Pacific oyster (Crassostrea gigas) infected with ostreid herpes virus type 1. Aquaculture 445, 57–62.Google Scholar
Petton, B, Pernet, F, Robert, R and Boudry, P (2013) Temperature influence on pathogen transmission and subsequent mortalities in juvenile Pacific oysters Crassostrea gigas. Aquaculture Environment Interactions 3, 257–273.Google Scholar
Prado-Alvarez, M, Darmody, G, Hutton, S, O'Reilly, A, Lynch, SA and Culloty, SC (2016) Occurrence of OsHV-1 in Crassostrea gigas cultured in Ireland during an exceptionally warm summer. Selection of less susceptible oysters. Frontiers in Physiology 7, 492.Google Scholar
Renault, T (1998) Infections herpeétiques chez les invertébrés: détection de virus de type herpès chez les mollusques bivalves marins. Virologie 2, 401–403.Google Scholar
Renault, T and Arzul, I (2001) Herpes-like virus infections in hatchery-reared bivalve larvae in Europe: specific viral DNA detection by PCR. Journal of Fish Diseases 24, 161–167.Google Scholar
Renault, T and Lipart, C (1998) Diagnosis of herpes-like virus infections in oysters using molecular techniques. European Aquaculture Society, Special Publication 26, 235–236.Google Scholar
Renault, T and Novoa, B (2004) Viruses infecting bivalve molluscs. Aquatic Living Resources 17, 397–409.CrossRefGoogle Scholar
Renault, T, Cochennec, N, Le Deuff, RM and Chollet, B (1994a) Herpes-like virus infecting Japanese oyster (Crassostrea gigas) spat. Bulletin of the European Association of Fish Pathologists 14(2), 64–66.Google Scholar
Renault, T, Le Deuff, RM, Chollet, B, Cochennec, N and Gérard, A (2000) Concomitant herpes-like virus infections in hatchery-reared larvae and nursery-cultured spat Crassostrea gigas and Ostrea edulis. Diseases of Aquatic Organisms 42, 173–183.Google Scholar
Renault, T, Lipart, C and Arzul, I (2001) A herpes-like virus infects a non-ostreid bivalve species: virus replication in Ruditapes philippinarum larvae. Diseases of Aquatic Organisms 45, 1–7.CrossRefGoogle ScholarPubMed
Renault, T, Bouquet, AL, Maurice, JT, Lupo, C and Blachier, P (2014) Ostreid herpesvirus 1 infection among pacific oyster (Crassostrea gigas) spat: relevance of water temperature to virus replication and circulation prior to the onset of mortality. Applied and Environmental Microbiology 80, 17, 5419–5426.Google Scholar
Roque, A, Carrasco, N, Andree, KB, Lacuesta, B, Elandaloussi, L, Gairin, I, Rodgers, CJ and Furones, MD (2012. First report of OsHV-1 microvar in Pacific oyster (Crassostrea gigas) cultured in Spain. Aquaculture 324–325, 303–306.Google Scholar
Sauvage, C, Pépin, JF, Lapègue, S, Boudry, P and Renault, T (2009) Ostreid herpes virus 1 infection in families of the Pacific oyster, Crassostrea gigas, during a summer mortality outbreak: Differences in viral DNA detection and quantification using real-time PCR. Virus Research 142, 181–187.CrossRefGoogle ScholarPubMed
Segarra, A, Pépin, JF, Arzul, I, Morga, B, Faury, N and 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 Research 153, 92–99.Google Scholar
Segarra, A, Baillon, L, Faury, N, Delphine, T and Renault, T (2016) Detection and distribution of ostreid herpesvirus 1 in experimentally infected Pacific oyster spat. Journal of Invertebrate Pathology 133, 59–65.Google Scholar
Tan, J, Lancaster, M, Hyatt, A, van Driel, R, Wong, F and Warner, S (2008) Purification of a herpes-like virus from abalone (Haliotis spp.) with ganglioneuritis and detection by transmission electron microscopy. Journal of Virological Methods 149, 338–341.CrossRefGoogle ScholarPubMed
Venier, P, Varotto, L, Rosani, U, Millino, C, Celegato, B, Bernante, F, Lanfranchi, G, Novoa, B, Roch, P, Figueras, A and Pallavicini, A (2011) Insights into the innate immunity of the Mediterranean mussel Mytilus galloprovincialis. BMC Genomics 12, 69.Google Scholar
Viana, M, Mancy, R, Biek, R, Cleaveland, S, Cross, PC, Lloyd-Smith, JO and Haydon, DT (2014) Assembling evidence for identifying reservoirs of infection. Trends in Ecology & Evolution 29(5), 270–279.Google Scholar
Walsh, SW, Metzger, DA and Higuchi, R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 30th Anniversary Gem Vol. 54, No. 3. Reprinted from BioTechniques 10(4), 506–513.Google Scholar
Witte, BD, Devriese, L, Bekaert, K, Hoffman, S, Vandermeersch, G, Cooreman, K and Robbens, J (2014) Quality assessment of the blue mussel (Mytilus edulis): comparison between commercial and wild types. Marine Pollution Bulletin 85, 146–155.Google Scholar

ONLINE REFERENCES

Basic Local Alignment Search Tool (https://blast.ncbi.nlm.nih.gov).Google Scholar
Food and Agriculture Organization of the United Nations (FAO) (2015) (www.fao.org/fishery/culturedspecies/Crassostrea_gigas/en).Google Scholar
Marine Institute (www.marine.ie).Google Scholar
Met Éireann (www.met.ie).Google Scholar
OIE – Manual of Diagnostic Tests for Aquatic Animals: Infection with ostreid herpesvirus 1 microvariants (www.oie.int/fileadmin/Home/eng/Health_standards/aahm/current/chapitre_ostreid_herpesvirus_1.pdf).Google Scholar