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Contribution to the understanding of the cycle of the protozoan parasite Marteilia refringens

Published online by Cambridge University Press:  11 October 2013

I. ARZUL ,
B. CHOLLET ,
S. BOYER ,
D. BONNET ,
J. GAILLARD ,
Y. BALDI ,
M. ROBERT ,
J. P. JOLY ,
C. GARCIA  and
M. BOUCHOUCHA
I. ARZUL*
Affiliation:
IFREMER SG2M-LGPMM, Laboratory of Genetics and Pathology of Marine Molluscs, 17390 La Tremblade, France
B. CHOLLET
Affiliation:
IFREMER SG2M-LGPMM, Laboratory of Genetics and Pathology of Marine Molluscs, 17390 La Tremblade, France
S. BOYER
Affiliation:
Laboratoire EcoSym, UMR5119, Université Montpellier 2, CC 093, Place Eugène Bataillon, 34095 Montpellier Cedex 05, France
D. BONNET
Affiliation:
Laboratoire EcoSym, UMR5119, Université Montpellier 2, CC 093, Place Eugène Bataillon, 34095 Montpellier Cedex 05, France
J. GAILLARD
Affiliation:
IFREMER SG2M-LGPMM, Laboratory of Genetics and Pathology of Marine Molluscs, 17390 La Tremblade, France
Y. BALDI
Affiliation:
IFREMER Laboratory Environment and Resource Provence Azur Corse, 20600 Bastia, France
M. ROBERT
Affiliation:
IFREMER SG2M-LGPMM, Laboratory of Genetics and Pathology of Marine Molluscs, 17390 La Tremblade, France
J. P. JOLY
Affiliation:
IFREMER SG2M-LGPMM, Laboratory of Genetics and Pathology of Marine Molluscs, 17390 La Tremblade, France
C. GARCIA
Affiliation:
IFREMER SG2M-LGPMM, Laboratory of Genetics and Pathology of Marine Molluscs, 17390 La Tremblade, France
M. BOUCHOUCHA
Affiliation:
IFREMER Laboratory Environment and Resource Provence Azur Corse, 83507 La Seyne/Mer Cedex, France
*
* Corresponding author. IFREMER, Laboratory of Genetics and Pathology, Av de Mus de Loup, 17390 La Tremblade, France. E-mail: [email protected]
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Summary

The paramyxean parasite Marteilia refringens infects several bivalve species including European flat oysters Ostrea edulis and Mediterranean mussels Mytilus galloprovincialis. Sequence polymorphism allowed definition of three parasite types ‘M’, ‘O’ and ‘C’ preferably detected in oysters, mussels and cockles respectively. Transmission of the infection from infected bivalves to copepods Paracartia grani could be experimentally achieved but assays from copepods to bivalves failed. In order to contribute to the elucidation of the M. refringens life cycle, the dynamics of the infection was investigated in O. edulis, M. galloprovincialis and zooplankton over one year in Diana lagoon, Corsica (France). Flat oysters appeared non-infected while mussels were infected part of the year, showing highest prevalence in summertime. The parasite was detected by PCR in zooplankton particularly after the peak of prevalence in mussels. Several zooplanktonic groups including copepods, Cladocera, Appendicularia, Chaetognatha and Polychaeta appeared PCR positive. However, only the copepod species Paracartia latisetosa showed positive signal by in situ hybridization. Small parasite cells were observed in gonadal tissues of female copepods demonstrating for the first time that a copepod species other than P. grani can be infected with M. refringens. Molecular characterization of the parasite infecting mussels and zooplankton allowed the distinguishing of three Marteilia types in the lagoon.

Keywords

bivalvescopepodsMarteilia refringensParacartia latisetosaparasite life cyclezooplankton
Type
Research Article
Information
Parasitology , Volume 141 , Issue 2 , February 2014 , pp. 227 - 240
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Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Alderman, D. J. (1979). Epizootiology of Marteilia refringens in Europe. Marine Fisheries Review 41, 67–69.Google Scholar
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, 3389–3402.Google Scholar
Andral, B. and Sargian, P. (2010). Directive Cadre Eau – District « Corse » Contrôles de surveillance/opérationnel (campagne DCE 2009) RST.DOPLER/PAC/10-20, décembre 2010.Google Scholar
Audemard, C., Barnaud, A., Collins, C. M., Le Roux, F., Sauriau, P. G., Coustau, C., Blachier, P. and Berthe, F. C. J. (2001). Claire ponds as an experimental model for Marteilia refringens life-cycle studies: new perspectives. Journal of Experimental Marine Biology and Ecology 257, 87–108.Google Scholar
Audemard, C., Le Roux, F., Barnaud, A., Collins, C., Sautour, B., Sauriau, P. G., De Montaudouin, X., Coustau, C., Combes, C. and Berthe, F. (2002). Needle in a haystack: involvement of the copepoda Paracartia grani in the life-cycle of the oyster pathogen Marteilia refringens . Parasitology 124, 315–323.Google Scholar
Balouet, G., Chaste, C., Cahour, A., Quillard, A. and Poder, M. (1979). Etude épidémiologique et pathologique de la maladie de l'huître plate en Bretagne. Bulletin de l'Institut des Pêches Maritimes 289, 13–23.Google Scholar
Balseiro, P., Montes, A., Ceschia, G., Gestal, C., Novoa, B. and Figueras, A. (2007). Molecular epizootiology of the European Marteilia spp., infecting mussels (Mytilus galloprovincialis and M. edulis) and oysters (Ostrea edulis): an update. Bulletin of the European Association of Fish Pathologists 27, 148–156.Google Scholar
Berthe, F. C. J., Pernas, M., Zerabib, M., Haffner, P., Thebault, A. and Figueras, A. J. (1998). Experimental transmission of Marteilia refringens with special consideration of its life cycle. Diseases of Aquatic Organisms 34, 135–144.Google Scholar
Berthe, F. C. J., Le Roux, F., Peyretaillade, E., Peyret, P., Rodriguez, D., Gouy, M. and Vivares, C. P. (2000). The existence of the phylum Paramyxea Desportes and Perkins, 1990 is validated by the phylogenetic analysis of the Marteilia refringens small subunit ribosomal RNA. Journal of Eukaryotic Microbiology 47, 288–293.CrossRefGoogle ScholarPubMed
Boyer, S., Arzul, I. and Bonnet, D. (2012). Some like it hot: Paracartia grani (Copepoda: Calanoida) arrival in the Thau lagoon (south of France-Mediterranean Sea). Marine Biodiversity Records. doi: 10.1017/S1755267212000565.Google Scholar
Burreson, E. M. (2008). Misuse of PCR assay for diagnosis of mollusc protistan infections. Diseases of Aquatic Organisms 80, 81–83. doi: 10.3354/dao01925.CrossRefGoogle ScholarPubMed
Carrasco, N., López-Flores, I., Alcaraz, M., Furones, M. D., Berthe, F. C. J. and Arzul, I. (2007 a). Dynamics of the parasite Marteilia refringens (Paramyxea) in Mytilus galloprovincialis and zooplankton populations in Alfacs Bay (Catalonia, Spain). Parasitology 134, 1541–1550. doi: 10.1017/S0031182007003009.Google Scholar
Carrasco, N., López-Flores, I., Alcaraz, M., Furones, M. D., Berthe, F. C. J. and Arzul, I. (2007 b). First record of a Marteilia parasite (Paramyxea) in zooplankton populations from a natural estuarine environment. Aquaculture 269, 63–70.Google Scholar
Carrasco, N., Arzul, I., Chollet, B., Robert, M., Joly, J.-P., Furones, D. and Berthe, F. C. J. (2008 a). Comparative experimental infection of the copepod Paracartia grani with Marteilia refringens and Marteilia maurini . Journal of Fish Diseases 31, 497–504. doi: 10.1111/j.1365-2761.2008.00910.x. Google Scholar
Carrasco, N., Arzul, I., Berthe, F. C. J., Fernàndez-Tejedor, M., Dufort, M. and Furones, M. D. (2008 b ). Delta de l'Ebre is a natural bay model for Marteilia spp. (Paramyxea) dynamics and life-cycle studies. Diseases of Aquatic Organisms 79, 65–73. doi: 10.3354/dao01844.Google Scholar
Carrasco, N., Andree, K. B., Lacuesta, B., Roque, A., Rodgers, C. and Furones, M. D. (2012). Molecular characterization of the Marteilia parasite infecting the common edible cockle Cerastoderma edule in the Spanish Mediterranean coast. A new Marteilia species affecting bivalves in Europe. Aquaculture 324–325, 20–26. doi: 10.1016/j.aquaculture.2011.10.017.Google Scholar
Casabianca, M. L., Kiener, A. and Huvé, H. (1973). Biotopes et biocénoses des étangs saumâtres corses: Biguglia, Diana, Urbino, Palo. Vie et Milieu, 23(2-C), 187–227.Google Scholar
Comps, M. (1970). Observations sur les causes d'une mortalité anormale des huîtres plates dans le bassin de Marennes. Revue des Travaux de l'Institut des Pêches Maritimes 34, 317–326.Google Scholar
Comps, M., Grizel, H. and Papayanni, Y. (1982). Infection parasitaire causée par Marteilia maurini sp. n chez la moule Mytilus galloprovincialis. CIEM C.M. 1982/F:24:3 pp.Google Scholar
Comps, M., Park, M. S. and Desportes, I. (1986). Ultrastructural study of Marteilioides chungmuensis gen. nov., sp. nov., a parasite of the ovocytes of the oyster Crassostrea gigas Th. Protistologica 22, 279–285.Google Scholar
Figueras, A. J. and Robledo, J. A. F. (1993). Does the Marteilia present in mussels (Mytilus galloprovincialis) infect flat oyster (Ostrea edulis)? Bulletin of the European Association of Fish Pathologists 13, 97–99.Google Scholar
Ginsburger-Vogel, T. and Desportes, I. (1979). Etude ultrastructurale de la sporulation de Paramarteilia orchestiae gen. N. sp.n. parasite de l'amphipode Orchestia gammarellus . Marine Fishery Review 41, 3–7.Google Scholar
Goulletquer, P. and Héral, M. (1997). Marine molluscan production trends in France: from fisheries to aquaculture. NOAA Technical Report NMFS series 129, 137–164.Google Scholar
Grizel, H. (1985). Etudes des récentes épizooties de l'huître plate Ostrea edulis L. et de leur impact sur l'ostréiculture bretonne. Ph.D. dissertation. Université des Sciences et Techniques de Languedoc, Montpellier, France.Google Scholar
Grizel, H. and Tigé, G. (1973) La maladie de la glande digestive d'Ostrea edulis Linné. CIEM C.M.1973/K:13:7 pp.Google Scholar
Grizel, H., Comps, M., Cousseraris, F., Bonami, J. R. and Vago, C. (1974). Etude d'un parasite de la glande digestive observé au cours de l’épizootie actuelle de l'huître plate. Compte Rendu de l'Académie des Sciences Série D Paris 279, 783–784.Google Scholar
Howard, A. W. and Smith, C. S. (1983). Histological techniques for marine bivalve mollusks. NOAA Technical Memorandum NMFS-F/NEC-25, Woods Hole.Google Scholar
Le Roux, F., Audemard, C., Barnaud, A. and Berthe, F. (1999). DNA probes as potential tools for the detection of Marteilia refringens . Marine Biotechnology 1, 588–597.Google Scholar
Le Roux, F., Lorenzo, G., Peyret, P., Audemard, C., Figueras, A., Vivares, C., Gouy, M. and Berthe, F. (2001). Molecular evidence for the existence of two species of Marteilia in Europe. Journal of Eukaryotic Microbiology 48, 449–454.Google Scholar
Longshaw, M., Feist, S. W., Matthews, A. and Figueras, A. (2001). Ultrastructural characterisation of Marteilia species (Paramyxea) from Ostrea edulis, Mytilus edulis and Mytilus galloprovincialis in Europe. Diseases of Aquatic Organisms 44, 137–142.Google Scholar
Lopez-Flores, I., de la Herran, R., Garrido-Ramos, M. A., Navas, J. I., Ruiz-Rejon, C. and Ruiz Rejon, M. (2004). The molecular diagnosis of Marteilia refringens and differentiation between Marteilia strains infecting oysters and mussels based on the rDNA IGS sequence. Parasitology 12, 411–419. doi: 10.1017/S0031182004005827.CrossRefGoogle Scholar
Meuriot, E. and Grizel, H. (1984). Note sur l'impact economique des maladies de l'huître plate en Bretagne. Rapport Technique I.S.T.P.M. 12:19 pp.Google Scholar
Novoa, B., Posada, D. and Figueras, A. (2005). Polymorphisms in the sequences of Marteilia internal transcribed spacer region of the ribosomal RNA genes (ITS-1) in Spain: genetic types are not related with bivalve hosts. Journal of Fish Diseases 2, 331–338. doi: 10.1111/j.1365-2761.2005.00634.x.CrossRefGoogle Scholar
OIE, Office International des Epizooties (2011). Aquatic Animal Health Code, 79th Edn. OIE, Paris.Google Scholar
OSPAR agreement 2008-6. Ospar convention for the protection of the marine environment of the northeast Atlantic. www.ospar.org/html_documents/ospar/html/ospar_list_of_decsrecs.pdf.Google Scholar
Pichot, Y. (2002). Bilan de l’état zoosanitaire des mollusques en méditerranée française 1988–2001. DRV/RST/RA/LCM/2002-11, 36 pp.Google Scholar
R Core Development Team (2009). R: a language and environment for statistical computing version 2.12.1. http://www.r-project.org.Google Scholar
REPAMO (2005). Bilan 2004 du réseau REPAMO (Réseau national de surveillance zoosanitaire des mollusques marins). 69 pp.Google Scholar
REPAMO (2007). Bilan 2006 du réseau REPAMO (Réseau national de surveillance zoosanitaire des mollusques marins). 38 pp.Google Scholar
Robledo, J. A. F. and Figueras, A. J. (1995). The effects of culture-site, depth, season and stock source on the prevalence of Marteilia refringens in cultured mussels (Mytilus galloprovincialis Lmk.) from Galicia. Spain. Journal of Parasitology 81, 354–363.Google Scholar
Saitou, N. and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Tajima, F. and Nei, M. (1984). Estimation of evolutionary distance between nucleotide sequences. Molecular Biology and Evolution 1, 269–285.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, 2731–2739. doi: 10.1093/ molbev/msr121.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acid Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Villalba, A., Mourelle, S. G., López, M. C., Carballal, M. J. and Azevedo, C. (1993). Marteiliasis affecting cultured mussels Mytilus galloprovincialis of Galicia (NW Spain). Etiology, phases of the infection, and temporal and spatial variability in prevalence. Diseases of Aquatic Organisms 16, 61–72.Google Scholar
Virvilis, C., Angelidis, P. and Photis, G. (2003). Presence of the parasite Marteilia sp. in the shellfish of the Thermaikos gulf in northern Greece. Bulletin of the European Association of Fish Pathologists 23, 157–162.Google Scholar
Zrncic, S., Le Roux, F., Oraic, D., Sostaric, B. and Berthe, F. C. J. (2001). First record of Marteilia sp in mussels Mytilus galloprovincialis in Croatia. Diseases of Aquatic Organisms 44, 143–148.Google Scholar