Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-26T06:25:26.042Z Has data issue: false hasContentIssue false

One Perkinsus species may hide another: characterization of Perkinsus species present in clam production areas of France

Published online by Cambridge University Press:  16 August 2012

I. ARZUL*
Affiliation:
IFREMER, Laboratory of Genetics and Pathology, Av de Mus de Loup-17390, La Tremblade, France
B. CHOLLET
Affiliation:
IFREMER, Laboratory of Genetics and Pathology, Av de Mus de Loup-17390, La Tremblade, France
J. MICHEL
Affiliation:
IFREMER, Laboratory of Genetics and Pathology, Av de Mus de Loup-17390, La Tremblade, France
M. ROBERT
Affiliation:
IFREMER, Laboratory of Genetics and Pathology, Av de Mus de Loup-17390, La Tremblade, France
C. GARCIA
Affiliation:
IFREMER, Laboratory of Genetics and Pathology, Av de Mus de Loup-17390, La Tremblade, France
J.-P. JOLY
Affiliation:
IFREMER, Laboratory of Genetics and Pathology, Av de Mus de Loup-17390, La Tremblade, France
C. FRANÇOIS
Affiliation:
IFREMER, Laboratory of Genetics and Pathology, Av de Mus de Loup-17390, La Tremblade, France
L. MIOSSEC
Affiliation:
IFREMER, Department of Data Development, Integrated Management and Survey, rue de l'île d'Yeu BP 21105-44311, Nantes Cedex 03, France
*
*Corresponding author: IFREMER, Laboratory of Genetics and Pathology, Av de Mus de Loup-17390, La Tremblade, France. Tel: 00 33 5 46 76 26 10. Fax : 00 33 5 46 75 26 11. E-mail : Isabelle.arzul@ifremer.fr

Summary

Although clam populations in France are known to be infected with protozoans of the genus Perkinsus, no molecular characterization was previously performed on these parasites. Considering that several members of this genus have been associated with mortalities of molluscs worldwide, a study was undertaken in order to characterize these parasites in France. For that purpose, clams, Ruditapes philippinarum and R. decussatus, collected from different production areas and found to be infected with Perkinsus sp. in thioglycolate culture medium, were selected for PCR-RFLP tests and sequencing. Perkinsus olseni was detected in all the investigated areas and results also suggested the presence of P. chesapeaki in Leucate, a lagoon on the Mediterranean coast and in Bonne Anse in Charente Maritime, on the Atlantic coast. Clonal cultures from both detected species were produced in order to describe and compare in vitro stages. Differences in size between both Perkinsus spp. were noticed especially for schizonts and zoosporangia. Lastly, in situ hybridization tests allowed confirmation of the presence of both species in the same R. decussatus population and even in same clams. This is the first detection of P. chesapeaki in Ruditapes species and outside North America, which questions its introduction into Europe.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

Abollo, E., Casas, S. M., Ceschia, G. and Villalba, A. (2006). Differential diagnosis of Perkinsus species by polymerase chain reaction-restriction fragment length polymorphism assay. Molecular and Cellular Probes 20, 323329. doi :10.1016/j.aquaculture.2011.10.017CrossRefGoogle ScholarPubMed
Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein data base search programs. Nucleic Acids Research 25, 33893402.CrossRefGoogle Scholar
Azevedo, C. (1989). Fine structure of Perkinsus atlanticus n. sp. (Apicomplexa, Perkinsea) parasite of clams, Ruditapes decussatus, from Portugal. Journal of Parasitology 75, 627635.CrossRefGoogle Scholar
Bascheri, M. C. (1965). Essai d'acclimatation du clam, Venus mercenaria, en milieu lagunaire méditerranéen (note préliminaire). Rapport du Commité International de la Mer Mediterranée, CIEM 18, 703714.Google Scholar
Bower, S. M., Blackbourn, J. and Meyer, G. R. (1998). Distribution, prevalence, and pathogenicity of the protozoan Perkinsus qugwadi in Japanese scallops, Patinopecten yessoensis, cultured in British Columbia, Canada. Canadian Journal of Zoology 76, 954959.CrossRefGoogle Scholar
Burreson, E. M., Reece, K. S. and Dungan, C. F. (2005). Molecular, Morphological, and Experimental Evidence Support the Synonymy of Perkinsus chesapeaki and Perkinsus andrewsi. The Journal of Eukaryotic Microbiology 52, 258270. doi : 10.1111/j.1550-7408.2005.05-00035.xCrossRefGoogle ScholarPubMed
Bushek, D., Landau, B. and Scarpa, E. (2008). Perkinsus chesapeaki in stout razor clams Tagelus plebeius from Delaware Bay. Diseases of Aquatic Organisms 78, 243247.CrossRefGoogle ScholarPubMed
Casas, S. M., Grau, A., Reece, K. S., Apakupakul, K., Azevado, C. and Villalba, A. (2004). Perkinsus mediterraneus n. sp., a protistan parasite of the European flat oyster Ostrea edulis from the Balearic Islands, Mediterranean Sea. Diseases of Aquatic Organisms 58, 231244.CrossRefGoogle Scholar
Casas, S. M., Villalba, A. and Reece, K. S. (2002). Study of the perkinsosis of the carpet shell clam Tapes decussatus in Galicia (NW Spain). I. Identification of the etiological agent and in vitro modulation of zoosporulation by temperature and salinity. Diseases of Aquatic Organisms 50, 5165.CrossRefGoogle Scholar
Choi, K.-S., Park, K.-I.Lee, K.-W. and Matsuoka, K. (2002). Infection intensity, prevalence, and histopathology of Perkinsus sp. in the Manila clam, Ruditapes philippinarum, in Isahaya Bay, Japan. Journal of Shellfish Research 21, 119125.Google Scholar
Cigarría, J., Rodríguez, C. and Fernández, J. M. (1997). Impact of Perkinsus sp. on Manila clam Ruditapes philippinarum beds. Diseases of Aquatic Organisms 29, 117120.CrossRefGoogle Scholar
Coss, C. A., Robledo, J. A. F., Ruiz, J. M. and Vasta, G. R. (2001 b). Description of Perkinsus andrewsi n. sp. isolated from the Baltic clam (Macoma balthica) by characterization of the ribosomal RNA locus, and development of a species-specific PCR-based diagnostic assay. The Journal of Eukaryotic Microbiology 48, 5261. doi: 10.1111/j.1550-7408.2001.tb00415.xCrossRefGoogle Scholar
Coss, C. A., Robledo, J. A. F. and Vasta, G. R. (2001 a). Fine structure of clonally propagated in vitro life stages of a Perkinsus sp. isolated from the Baltic clam Macoma balthica. The Journal of Eukaryotic Microbiology 48, 3851. doi: 10.1111/j.1550-7408.2001.tb00414.xCrossRefGoogle ScholarPubMed
Dang, C., de Montaudouin, X., Gonzalez, P., Mesmer-Dudons, N. and Caill-Milly, N. (2008). Brown muscle disease (BMD), an emergent pathology affecting Manila clam Ruditapes philippinarum in Arcachon Bay (SW France). Diseases of Aquatic Organisms 80, 219228.CrossRefGoogle ScholarPubMed
Dang, C., de Montaudouin, X., Caill-Milly, N. and Željka, T. (2010). Spatio-temporal patterns of perkinsosis in the Manila clam Ruditapes philippinarum from Arcachon Bay (SW France). Diseases of Aquatic Organisms 91, 151159.CrossRefGoogle ScholarPubMed
D'Hardivillé, C., Bouché, L. and Péronnet, I. (2010 a). Campagne d’évaluation du stock de palourdes de la baie de Vilaine (Pénestin), 16–17 mars 2010. Rapport Ifremer Comité Local des Pêches Maritimes et des élevages marins Auray-Vannes, France.Google Scholar
D'Hardivillé, C., Bouché, L. and Péronnet, I. (2010 b). Campagne d’évaluation du stock de palourdes du Golfe du Morbihan, 10–15 mars 2010. Rapport Ifremer Comité Local des Pêches Maritimes et des élevages marins Auray-Vannes, France.Google Scholar
Dungan, C. F., Hamilton, R. M., Hudson, K. L., McCollough, C. B. and Reece, K. S. (2002). Two epizootic diseases in Chesapeake Bay commercial clams Mya arenaria and Tagelus plebeius. Diseases of Aquatic Organisms 50, 6778.CrossRefGoogle ScholarPubMed
Dungan, C. F. and Reece, K. S. (2006). In vitro propagation of two Perkinsus spp. parasites from Japanese Manila clams Venerupis philippinarum and description of Perkinsus honshuensis n. sp. The Journal of Eukaryotic Microbiology 53, 316326. doi: 10.1111/j.1550-7408.2006.00120.xCrossRefGoogle ScholarPubMed
Elandaloussi, L., Carrasco, N., Furones, D. and Roque, A. (2009). Phylogenetic relationship of Perkinsus olseni from the Ebro Delta, Spain, to other Perkinsus species, based on ribosomal DNA sequences. Diseases of Aquatic Organisms 86, 135142.CrossRefGoogle ScholarPubMed
Food and Agriculture Organization of the United Nations (FAO) (2009). FishStat Plus -Universal Software for Fishery Statistical Time Series. Accessed 26 January, 2011. http://www.fao.org/fi/statist/FISOFT/FISHPLUS.aspGoogle Scholar
Figueras, A, Robledo, J. A. F. and Novoa, B. (1992). Occurrence of haplosporidian and Perkinsus-like infections in carpet-shell clams, Ruditapes decussatus, of the Ria de Vigo (Galicia NW Spain). Journal of Shellfish Research 11, 377382.Google Scholar
Figueras, A., Robledo, J. A. F. and Novoa, B. (1996). Brown ring disease and parasites in clams (Ruditapes decussatus and R. philippinarum) from Spain and Portugal. Journal of Shellfish Research 15, 363368.Google Scholar
Garcia, C., Arzul, I., Chollet, B., François, C., Goubet, A., Joly, J. P., Miossec, L. and Robert, M. (2006). Bilan 2005 du réseau REPAMO. Rapport Ifremer, LGP, La Tremblade, France.Google Scholar
Gauthier, J. D. and Vasta, G. R. (1995). In vitro culture of the eastern oyster parasite Perkinsus marinus: optimization of the methodology. Journal of Invertebrate Pathology 66, 156168.CrossRefGoogle Scholar
Goggin, C. L. (1992) Occurrence of parasites of the genus Perkinsus in France. Bulletin of the European Association of Fish Patholology 12, 174176.Google Scholar
Goggin, C. L. and Lester, R. J. G. (1995). Perkinsus, a protistan parasite of abalone in Australia: a review. Australian Journal of Marine and Freshwater Resources 46, 639646.CrossRefGoogle Scholar
Goulletquer, P., Bachelet, G., Sauriau, P.-G. and Noel, P. (2002). Open Atlantic coast of Europe – a century of introduced species into french waters. In Invasive Aquatic Species of Europe (ed. Leppäkkosski, E., Gollasch, S. and Olenin, S.), pp. 276290. Kluwer Academic Publishers, The Netherlands.Google Scholar
Lambert, L. (1947–1949). Note complémentaire sur le clam (Venus mercenaria). Revue des Travaux de l'Office des Pêches Maritimes 15, 118122.Google Scholar
Lassalle, G., de Montaudouin, X., Soudant, P. and Paillard, C. (2007). Parasite co-infection of two sympatric bivalves, the Manila clam (Ruditapes philippinarum) and the cockle (Cerastoderma edule) along a latitudinal gradient. Aquatic Living Resources 20, 3342. doi: 10.1051/alr:2007013CrossRefGoogle Scholar
Lenaers, G., Maroteaux, L., Michot, B. and Herzog, M. (1989). Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosomal RNA. Journal of Molecular Evolution 29, 4051.CrossRefGoogle ScholarPubMed
Lester, R. J. G. and Davis, G. H. G. (1981). A new Perkinsus species (Apicomplexa, Perkinsea) from the abalone Haliotis ruber. Journal of Invertebrate Pathology 37, 181187.CrossRefGoogle Scholar
McLaughlin, S. M. and Faisal, M. (2000). Prevalence of Perkinsus spp. in Chesapeake Bay soft-shell clams, Mya arenaria Linnaeus, 1758 during 1990–1998. Journal of Shellfish Research 19, 349352.Google Scholar
McLaughin, S. M., Tall, B. D., Shaheen, A., Elsayed, E. E. and Faisal, M. (2000). Zoosporulation of a new Perkinsus species isolated from the gills of the softshell clam Mya arenaria. Parasite 7, 115122.CrossRefGoogle Scholar
Moss, J. A., Burreson, E. M. and Reece, K. S. (2006). Advanced Perkinsus marinus infections in Crassostrea ariakensis maintained under laboratory conditions. Journal of Shellfish Research 25, 6572. doi: 10.2983/0730-8000(2006)25[65:APMIIC]2.0.CO;2CrossRefGoogle Scholar
Moss, J. A., Xiao, J., Dungan, C. F. and Reece, K. S. (2008). Description of Perkinsus beihaiensis n. sp., a new Perkinsus sp. Parasite in Oysters of Southern China. The Journal of Eukaryotic Microbiology 55, 117130. doi: 10.1111/j.1550-7408.2008.00314.xCrossRefGoogle Scholar
Murrell, A., Kleeman, S. N., Barker, S. C. and Lester, R. J. G. (2002). Synonymy of Perkinsus olseni Lester & Davis, 1981 and Perkinsus atlanticus Azevedo, 1989 and an update on the phylogenetic position of the genus Prekinsus. Bulletin of the European Association of Fish Pathologists 22, 258265.Google Scholar
OIE, World Organisation for Animal Health (2011). Aquatic Animal Health Code. World Organisation for Animal Health, Paris, France.Google Scholar
Ordás, M. C. and Figueras, A. (1998). In vitro culture of Perkinsus atlanticus, a parasite of the carpet shell clam Ruditapes decussatus. Diseases of Aquatic Organisms 33, 129136.CrossRefGoogle Scholar
Paillard, C. (2004). A short-review of brown ring disease, a vibriosis affecting clams, Ruditapes philippinarum and Ruditapes decussatus. Aquatic Living Resources 17, 467475.CrossRefGoogle Scholar
Pecher, W. T., Robledo, J. A. and Vasta, G. R. (2004). Identification of a second rRNA gene unit in the Perkinsus andrewsi genome. The Journal of Eukaryotic Microbiology 51, 234245.CrossRefGoogle ScholarPubMed
Perkins, F. O. (1996). The structure of Perkinsus marinus (Mackin, Owen, and Collier, 1950) Levine, 1978, with comments on the taxonomy and phylogeny of Perkinsus sp. Journal of Shellfish Research 15, 6787.Google Scholar
Petersen, K. S., Rasmussen, K. L., Heinemeier, J. and Rud, N. (1992). Clams before Columbus? Nature, London 359, 679.CrossRefGoogle Scholar
Ray, S. M. (1996). Historical perspective on Perkinsus marinus disease of oysters in the Gulf of Mexico. Journal of Shellfish Research 15, 911.Google Scholar
Reece, K. S., Bushek, D. and Graves, J. E. (1997). Molecular markers for population genetic analysis of Perkinsus marinus. Molecular Marine Biology and Biotechnology 6, 197206.Google Scholar
Reece, K. S., Bushek, D., Hudson, K. L. and Graves, J. E. (2001). Geographic distribution of Perkinsus marinus genetic strains along the Atlantic and Gulf coasts of the USA. Marine Biology 139, 10471055. doi: 10.1007/s002270100657Google Scholar
Reece, K. S., Dungan, C. F. and Burreson, E. M. (2008). Molecular epizootiology of Perkinsus marinus and P. chesapeaki infections among wild oysters and clams in Chesapeake Bay, USA. Diseases of Aquatic Organisms 82, 237248.CrossRefGoogle ScholarPubMed
Robledo, J. A. F., Wright, A. C., Marsh, A. G. and Vasta, G. R. (1999). Nucleotide sequence variability in the nontranscribed spacer of the rRNA locus in the oyster parasite Perkinsus marinus. The Journal of Parasitology 85, 650656.CrossRefGoogle ScholarPubMed
Ruano, F. and Cachola, R. (1986). Outbreak of a severe epizootic of Perkinsus marinus (Levin-78) at Ria de Faro clam's culture beds. In Abstracts of the Second International Colloquium on Pathology in Marine Aquaculture (PAMAQ II) University of Oporto, Porto, Portugal, pp. 4142.Google Scholar
Ruckebusch, H. (1947–1949). Le clam. Note sur Venus mercenaria L. Son introduction et son élevage dans le bassin de la Seudre. Revue des Travaux de l'Office des Pêches Maritimes 15, 99117.Google Scholar
Sanchez, F., Caill-Milly, N., Lissardy, M., de Casamajor, M-N. and Morandeau, G. (2010). Campagne d’évaluation du stock de palourdes du bassin d'Arcachon, année 2010. Rapport Ifremer R.INT.DCN/HGS/LRHA 10-004.Google Scholar
Tajima, F. and Nei, M. (1984). Estimation of evolutionary distance between nucleotide sequences. Molecular Biology and Evolution 1, 269285.Google ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739. doi: 10.1093/molbev/msr121CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acid Research 22, 46734680.CrossRefGoogle ScholarPubMed
Vilas, R., Cao, A., Pardo, B. G., Fernandez, S. B., Villalba, A. and Martinez, P. (2011). Very low microsatellite polymorphism and large heterozygote deficits suggest founder effects and cryptic structure in the parasite Perkinsus olseni. Infection, Genetics and Evolution 11, 904911. doi: 10.1016/j.meegid.2011.02.015.CrossRefGoogle ScholarPubMed
Villalba, A. (2008). Workshop for the Analysis of the Impact of Perkinsosis to the European Shellfish Industry. Centro de Investigacións Mariñas, Conseillería de Pesca e Asuntos Marítimos da Xunta de Galicia, Vilanova de Arousa, Spain.Google Scholar
Villalba, A., Casas, S. M., Lopez, C. and Carballal, M. J. (2005). Study of perkinsosis in the carpet shell clam Tapes decussatus in Galicia (NW Spain). II. Temporal pattern of disease dynamics and association with clam mortality. Diseases of Aquatic Organisms 65, 257267.CrossRefGoogle ScholarPubMed
Villalba, A., Lopez, M. C. and Carballal, M. J. (1993). Parasitos y alteraciones patologicas de tres especies de almeja Ruditapes decussatus, Venerupis pullastra y Venerupis rhomboides en las rias gallegas. In Actas del IV Congreso Nacional de Acuicultura, 21–24 September 1993. Vilanova de Arousa, (ed. Cervino, A., Landin, A., Coo de, A., Guerra, A. and Torre, M.), pp. 551556.Google Scholar