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Effect of infection by the protistan parasite Marteilia refringens on the enzyme activity and energy reserves of oyster Ostrea stentina (Payraudeau, 1826) in Tunisia

Published online by Cambridge University Press:  03 October 2016

Refka Elgharsalli*
Affiliation:
Institut National Agronomique de Tunisie, 43, Avenue Charles Nicolle, 1082 Tunis, Tunisia
Catherine Seguineau
Affiliation:
IFREMER, Laboratoire de Physiologie des Invertébrés, Centre de Brest, 29280 Plouzané, France
Isabelle Arzul
Affiliation:
IFREMER, Laboratoire de Génétique et Pathologie, avenue de Mus de Loup, 17390 La, Tremblade, France
Nejla Aloui-Bejaoui
Affiliation:
Institut National Agronomique de Tunisie, 43, Avenue Charles Nicolle, 1082 Tunis, Tunisia
Claudie Quere
Affiliation:
IFREMER, Laboratoire de Physiologie des Invertébrés, Centre de Brest, 29280 Plouzané, France
Jeanne Moal
Affiliation:
IFREMER, Laboratoire de Physiologie des Invertébrés, Centre de Brest, 29280 Plouzané, France
*
Correspondence should be addressed to: R. Elgharsalli, Institut National Agronomique de Tunisie, 43, Avenue Charles Nicolle, 1082 Tunis, Tunisia email: [email protected]

Abstract

This is the first study of the metabolic enzyme activity and energy state of the dwarf oyster Ostrea stentina (Payraudeau, 1826) in Tunisia and in the Mediterranean region. The main purpose of this study was to examine the modulation of the physiological status of the oyster O. stentina depending on the season and the presence of parasite Marteilia refringens. The prevalence of bonamiosis and marteiliosis were established by PCR. Bonamia exitiosa was detected only in 2.91% of oysters while the prevalence of M. refringens was 100% (30 Ind./30) in February and 93.93% (28 Ind./30) in March. A 42–87% mortality rate was reported during the study period. Biochemical analyses were carried out to evaluate the management of the energy resources in regard to the biochemical changes of lipids and carbohydrates. The enzyme activity of pyruvate kinase (PK), citrate synthase (CS) and cytochrome c oxidase (CCO) were measured and the mean level of enzyme activity was respectively 20.31 mU mg−1 protein; 12.06 mU mg−1 protein and 3.59 mU mg−1 protein. Carbohydrate contents of O. stentina were very low all year round with an average of 15.18% in dry weight, and lipid contents remain similar (11.77% in dry weight) compared with the values reported for most other temperate bivalves. Enzyme activity significantly decreased over time (P < 0.001). The energy resources of the oyster O. stentina wherein much of the energy was devoted to reproduction seem to affect the defence system.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Alderman, D.J. (1979) Epizootiology of Marteilia refringens in Europe. Marine Fishery Review 41, 6769.Google Scholar
Almeida, M.J., Machado, A. and Coimbra, J. (1997) Growth and biochemical composition of Crassostrea gigas (Thunberg) at three fishfarm earthen ponds. Journal of Shellfish Research 16, 455462.Google Scholar
Aloui-Bejaoui, N. (1998) Ecobiologie de la population de moules Mytilus galloprovincialis Lamark (1819) du lac de Bizerte. Thèse de Doctorat en Biologie. Université de Tunis II, Faculté des sciences de Tunis, 263 pp.Google Scholar
Barber, B.J. and Blake, N.J. (1991) Reproductive physiology. In Shumway, S. (ed.) Scallops: biology, ecology and aquaculture. Amsterdam: Elsevier, pp. 377428.Google Scholar
Bayne, B.L. (1976) The biology of mussel larvae. In Bayne, B.L. (ed.) Marine mussels: their ecology and physiology. Cambridge: Cambridge University Press, pp. 81120.Google Scholar
Ben Kheder, D.R. (2001) Contribution à l’étude ecobiologique de Donax trunculus, (Linnaeus, 1758) Mollusques Bivalves, dans le Golfe de Tunis – DEA. Université de Tunis, 104 pp.Google Scholar
Berthe, F., Le Roux, F., Adlard, R. and Figueras, A. (2004) Marteiliosis in molluscs: a review. Aquatic Living Resource 17, 433448.CrossRefGoogle Scholar
Berthelin, C., Kellner, K. and Mathieu, M. (2000) Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (West Coast of France). Compte Biochemical Physiology 12, 359369.Google Scholar
Bligh, E.G. and Dyer, W.J. (1959) A rapid method for total lipid extraction and purification. Compte Biochemical Physiology 37, 911917.Google Scholar
Carrasco, N., Arzul, I., Chollet, B., Robert, M., Joly, J.P., Furones, M.D. and Berthe, F.C.J. (2008) Comparative experimental infection of the copepod Paracartia grani with Marteilia refringens and Marteilia maurini . Journal of Fish Diseases 31, 497504.Google Scholar
Cochennec, N., Le Roux, F., Berthe, F. and Gérard, A. (2000) Detection of Bonamia ostreae based on small subunit ribosomal probe. Journal of Invertebrate Pathology 76, 2632.Google Scholar
Cochennec-Laureau, N., Reece, K.S., Berthe, F.C.J. and Hine, P.M. (2003) Mikrocytos roughleyi taxonomic affiliation leads to the genus Bonamia (Haplosporidia). Diseases of Aquatic Organisms 54, 209217.CrossRefGoogle Scholar
Comps, M., Pichot, Y. and Deltreil, J.P. (1979) Mise en évidence d'une microsporidie parasite Marteilia refrinfens agent de la maladie de la glande digesive d'Ostrea edulis . Revue des Travaux de l'Institut des Pêches Maritimes 43, 409412.Google Scholar
Comps, M., Pichot, Y. and Pagianni, P. (1982) Recherche sur Marteilia maurini n. sp. parasite de la moule Mytilus galloprovincialis LMK. Revue des Travaux de l'Institut des Pêches Maritimes 45, 211214.Google Scholar
Costil, K., Royer, J., Roport, M., Soletchnik, P. and Mathieu, M. (2005) Spatio-temporal variations in biological performances and summer mortality of the Pacific oyster Crassostrea gigas in Normandy (France). Helgoland Marine Research 59, 286300.Google Scholar
Dahlhoff, E.P., Stillman, J.H. and Menge, B.A. (2002) Physiological community ecology variation in metabolic activity of ecologically important rocky intertidal invertebrates along environmental gradients. Integrative and Comparative Biology 42, 862871.Google Scholar
Delaporte, M., Soudant, P., Lambert, C., Moal, J., Pouvreau, S. and Samain, J.F. (2006) Impact of food availability on energy storage and defense related hemocyte parameters of the Pacific oyster Crassostrea gigas during an experimental reproductive cycle. Aquaculture 254, 571582.Google Scholar
Deslous-Paoli, J.M. and Héral, M. (1988) Biochemical composition and energy value of Crassostrea gigas (Thunberg) cultured in the bay of Marennes-Oléron. Aquatic Living Resources 1, 239249.Google Scholar
Dridi, S., Romdhane, M.S. and Elcafsi, M. (2007) Seasonal variation in weight and biochemical composition of the Pacific oyster, Crassostrea gigas in relation to the gametogenic cycle and environmental conditions of the Bizerte lagoon, Tunisia. Aquaculture 6, 238248.Google Scholar
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. and Smith, F. (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350356.Google Scholar
Dunphy, B.J., Wells, R.M.G. and Jeffs, A.G. (2006) Oxygen consumption and enzyme activity of the subtidal flat oyster (Ostrea chilensis) and Pacific oyster (Crassostrea gigas): responses to temperature and starvation. Journal of Marine and Freshwater Research 40, 149158.CrossRefGoogle Scholar
Elgharsalli, R. and Aloui, B.N. (2011) First study in the Mediterranean of gametogenesis of the oyster Ostrea stentina (Payraudeau, 1826) in the Gulf of Hammamet. Cahier de Biologie Marine 52, 157169.Google Scholar
Elgharsalli, R., Bejaoui, N.A., Salah, A., Chollet, H.B., Joly, J.P., Robert, M., Couraleau, Y. and Arzul, I. (2013) Characterization of the protozoan parasite Marteilia refringens infecting the dwarf oyster Ostrea stentina in Tunisia. Journal of Invertebrate Pathology 112, 175183.Google Scholar
Gabbott, P.A. and Walker, A.J.M. (1971) Changes in the condition index and biochemical content of adult oysters (Ostrea edulis L.) maintained under hatchery conditions. Conseil International pour l’Éxploration de la Mer 34, 98105.Google Scholar
Goulletquer, P.P., Soletchnik, O., Le Moine, D., Razet, P., Geairon, N., Faury and Taillade, S. (1998) Summer mortality of the Pacific cupped oyster Crassostrea gigas in the Bay of Marennes-Oléron (France). ICES Statutory Meeting 1998, Mariculture Committee CM 1 998/CC: 14, 21 pp.Google Scholar
Greenway, S.C. and Storey, K.B. (1999) The effect of prolonged anoxia on enzyme activities in oysters (Crassostrea virginica) at different seasons. Journal of Experimental Marine Biology and Ecology 242, 259272.Google Scholar
Greenway, S.C. and Storey, K.B. (2000) Seasonal change and prolonged anoxia affect the kinetic properties of phosphofructokinase and pyruvate kinase in oysters. Journal of Comparative Physiology B170, 285293.Google Scholar
Greenway, S.C. and Storey, K.B. (2001) Effects of seasonal change and prolonged anoxia on metabolic enzymes of Littorina littorea . Canadian Journal of Zoology 79, 907915.Google Scholar
Grizel, H., Comps, M., Cousserans, 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 de Paris 279, 783785.Google Scholar
Hill, K.M., Carnegie, R.B., Bejaoui, N.A., Elgharsalli, R., White, D.M., Stokes, N.A. and Burreson, E.M. (2010) Observation of a Bonamia sp. infecting the oyster Ostrea stentina in Tunisia, and a consideration of its phylogenetic affinities. Journal of Invertebrate Pathology 103, 179185.Google Scholar
Hine, P.M., Cochennec-Laureau, N.F. and Berthe, C.J. (2001) Bonamia exitiosus sp. (Haplosporidia) infecting flat oysters Ostrea chilensis in New Zealand. Diseases of Aquatic Organisms 47, 6372.Google Scholar
Jeffs, A.G. and Hickman, R.W. (2000) Reproductive activity in a preepizootic wild population of the Chilean oyster, Ostrea chilensis, from southern New Zealand. Aquaculture 183, 241253.Google Scholar
Kang, C.K., Park, M.S., Lee, P.Y., Choi, W.J. and Lee, W.C. (2000) Seasonal variation in condition, reproductive activity, and biochemical composition of the Pacific oyster, Crassostrea gigas (Thunberg), in suspended culture in two coastal bays in Korea. Journal of Shellfish Research 19, 771778.Google Scholar
Le Moullac, G., Bacca, H., Huvet, A., Moal, J., Pouvreau, S. and Van Wormhoudt, A. (2007) Transcriptional regulation of pyruvate kinase and phosphoenolpyruvate carboxykinase in the adductor muscle of the oyster Crassostrea gigas during prolonged hypoxia. Journal of Experimental Zoology 307, 371382.CrossRefGoogle ScholarPubMed
Le Roux, F., Lorenzo, G., Peyret, P., Audemard, C., Figueras, A., Vivarès, G., Gouy, M. and Berthe, F.C.J. (2001) Molecular evidence for the existence of two species of Marteilia refringens in Europe. Journal of Eukaryotic Microbiology 48, 449454.Google Scholar
Li, Q., Osada, M. and Mori, K. (2000) Seasonal biochemical variations in Pacific oyster gonadal tissue during sexual maturation. Fisheries Sciences 66, 502508.Google Scholar
López-Flores, I., de la Herran, R., Garrido-Ramos, M.A., Navas, J.I., Ruiz-Rejón, C. and Ruiz-Rejón, M. (2004) The molecular diagnosis of Marteilia refringens and differentiation between Marteilia strains infecting oysters and mussels based on the rDNA IGS sequence. Parasitology 129, 411419.Google Scholar
Lowry, O.M., Rosenbrough, N.J., Farr, O.L. and Randall, R.J. (1951) Protein measurements with the folin reagents method. Journal of Biological Chemistry 193, 133145.CrossRefGoogle Scholar
Maurer, D. and Borel, M. (1986) Croissance, engraissement et cycle sexuel de Crassostrea gigas dans le bassin d'Arcachon: comparaison des huîtres âgées de 1 et 2 ans. Symp. SFM, Wimereux, Nov. 1985. Haliotis 15, 125134.Google Scholar
Mori, K. (1979) Effects of artificial eutrophication on the metabolism of the Japanese oyster C. gigas . Marine Biology 53, 361369.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 28, 331338.Google Scholar
OIE (2011) Aquatic animal health code. 79th ed. OIE, Paris: Office International des Epizooties.Google Scholar
Payraudeau, B.C. (1826) Catalogue descriptif et méthodique des annélides et de mollusques de l'Isle de Corse. Paris, 86 pp.Google Scholar
Pazos, A.J., Ruiz, C.O., Garcia, M., Abad, M. and Sanchez, J.L. (1996) Seasonal variations of the lipid content and fatty acid composition of Crassostrea gigas cultured in El Grove, Galicia, N.W. Spain. Comparative Biochemistry and Physiology 114B, 171179.Google Scholar
Perdue, J.A., Beattie, J.H. and Chew, K.K. (1981) Some relationships between gametogenic cycle and summer mortality phenomenon in the Pacific oyster (Crassostrae gigas) in Washington State. Journal of Shellfish Research 1, 916.Google Scholar
Robert, R., Borel, M., Pichot, Y. and Trut, G. (1991) Growth and mortality of the European oyster Ostrea edulis in the Bay of Arcachon (France). Aquatic Living Resources 4, 265274.Google Scholar
Samain, M.S., Mathieu, G., Vanderschaeve, L., Wanke, S., Neinhuis, C. and Goetghebeur, P. (2007) Nomenclature and typification of subdivisional names in the genus Peperomia (Piperaceae). Taxon 56, 229236.Google Scholar
Serve, P.A. (1969) Citrate synthase. In Lowenstein, J.M. (ed.) Methods in enzymology, Volume 13. New York, NY: Academic Press, pp. 311.Google Scholar
Soletchnik, P., Faury, N. and Goulletquer, P. (2006) Seasonal changes in carbohydrate metabolism and its relationship with summer mortality of Pacific oyster Crassostrea gigas (Thunberg) in Marennes-Ole'ron bay (France). Aquaculture 252, 328338.Google Scholar
Soletchnik, P., Goulletquer, P., Geairon, P. and Razet, D. (1996) Seuil de production de pseudo-féces de l'huître creuse du Pacifique: Crassostrea gigas (Thunberg) dans des conditions de faibles charges particulaires. Haliotis 25, 1324.Google Scholar
Sukhotin, A., Abele, D. and Pörtner, H. (2006) Ageing and metabolism of Mytilus edulis: populations from various climate regimes. Journal of Shellfish Research 24, 893899.Google Scholar
Tiscar, P.G., Zizzo, N. and Tempesta, M. (1991) Su alcune patologie riscontrate in ostriche piatte (Ostrea edulis) provenienti da banco naturale. Boll SIPI 7, 1318.Google Scholar
Tlig-Zouari, S. (1993) Contribution à l’étude ecobiologique de deux espèces de Mollusques lamellibranches Pinctada radiata (Leach, 1814) et Pinna nobilis (Linné 1758) des îles Kerkennah. Thèse de doctorat. Université de Tunis, 215 pp.Google Scholar
Villalba, A., Mourelle, S.G., Carballal, M.J. and Lopez, M.C. (1993b) Effects of infection by the protistan parasite Marteilia refringens on the reproduction of cultured mussels Mytilus galloprovincialis in Galicia (NW Spain). Diseases of Aquatic Organisms 17, 205213.Google Scholar
Virvilis, C. and Angelidis, P. (2006) Presence of the parasite Marteilia sp. in the flat oyster (Ostrea edulis L.) in Greece. Aquaculture 259, 15.Google Scholar
Wada, S.I., Iida, A., Akimoto, N., Kanai, M., Toyama, N. and Fujita, T. (1995) Fungal 597 metabolites. XIX. Structural elucidation of channel-forming peptides, Trichorovins - I- 598 XIV, from the fungus Trichoderma viridae . Chemical and Pharmaceutical Bulletin 43, 910915.Google Scholar
Wenne, R. and Polak, L. (1989) Lipid composition and storage in the tissues of the bivalve, Macoma balthica . Biochemical Systematics and Ecology 17, 583587.Google Scholar
Zandee, D.I., Kluytmans, J.H., Zurburg, W. and Pieters, H. (1980) Seasonal variations in biochemical composition of Mytilus edulis with reference to energy metabolism and gametogenesis. Netherlands Journal of Sea Research 14, 129.Google Scholar