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Effect of food supply on the detoxification in the blue mussel, Mytilus edulis, contaminated by diarrhetic shellfish toxins

Published online by Cambridge University Press:  24 December 2010

Claire Marcaillou ,
Joël Haure ,
Florence Mondeguer ,
Anne Courcoux ,
Béatrice Dupuy  and
Christian Pénisson
Claire Marcaillou*
Affiliation:
IFREMER, Dep. Environnement, Microbiologie & Phycotoxines, rue de l’Ile d’Yeu, BP 21105, 44311 Nantes, France
Joël Haure
Affiliation:
IFREMER, Station conchylicole des Pays de la Loire, Polder des Champs, 85230 Bouin, France
Florence Mondeguer
Affiliation:
IFREMER, Dep. Environnement, Microbiologie & Phycotoxines, rue de l’Ile d’Yeu, BP 21105, 44311 Nantes, France
Anne Courcoux
Affiliation:
IFREMER, Dep. Environnement, Microbiologie & Phycotoxines, rue de l’Ile d’Yeu, BP 21105, 44311 Nantes, France
Béatrice Dupuy
Affiliation:
IFREMER, Station conchylicole des Pays de la Loire, Polder des Champs, 85230 Bouin, France
Christian Pénisson
Affiliation:
IFREMER, Station conchylicole des Pays de la Loire, Polder des Champs, 85230 Bouin, France
*
a Corresponding author: claire.marcaillou@ifremer.fr
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Abstract

The objective of this study was to identify a possible effect of food on the acceleration of decontamination in blue mussels, Mytilus edulis, containing diarrhetic toxins belonging to the okadaic acid (OA) structural group. An experimental protocol was designed to describe and compare the decontamination kinetics and detoxification rates of naturally OA-contaminated mussels that had either received or not received food for three weeks. The protocol was applied in two trials (in June 2006 and June 2007, called Ker06 and Ker07), conducted one year apart on samples of mussels collected in the same area, at the same season. Okadaic acid (OA), the main lipophilic toxin produced by the toxic alga Dinophysis acuminata, was analysed over the course of the decontamination, in hydrolysed (total OA) and non hydrolysed (free OA) digestive gland extracts, in order to estimate acyl-esters (7-O-acyl-ester derivatives of OA) concentrations. OA analyses were also made for toxin presence in biodeposits and in the aqueous phase. Bivalve physiological status was evaluated by biomass measurements (dry weight of flesh) and two biochemical compounds (total lipid and glycogen concentrations). Measured physiological parameters showed that mussels did not suffer under experimental conditions. Both trials showed that the food accelerated the elimination of free and total OA. This effect cannot be attributed to a dilution of the toxin in the tissue, as results expressed in toxin burden led to the same conclusion. The kinetic models of decontamination differed between the two experiments: the model was linear for Ker06, provided that the values corresponding to the first two days were discarded, whereas data fitted a decreasing exponential curve better in Ker07. Detoxification rates increased as the food supply increased. After three weeks of experimentation, the detoxification rates for total OA in Ker06 and Ker07 were 52 and 61%, respectively, in unfed mussels and 90 and 89% in fed mussels (with the highest level in Ker07). Comparisons between the free OA and esters showed that detoxification rate was higher for free OA than for esters, whatever the level of food supply. The results of this study suggest that food increase probably accelerates elimination of OA and OA-esters but the latter are eliminated at a lower speed.

Keywords

MusselFeedingDigestive glandDepurationOkadaic acidAcyl estersMarine lipophilic biotoxinsMass spectrometry
Type
Research Article
Information
Aquatic Living Resources , Volume 23 , Issue 3 , July 2010 , pp. 255 - 266
Copyright
© EDP Sciences, IFREMER, IRD 2010

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References

Références

Blanco, J., Fernández, M.L., Miguez, A., Moroño, A., 1999, Okadaic acid depuration in the mussel Mytilus galloprovincialis: one- and two-compartment model and the effect of environmental conditions. Mar. Ecol. Prog. Ser. 176, 153–163. CrossRefGoogle Scholar
Blanco, J., Moroño, A., Fernández, M.L., 2005, Toxic episodes in shellfish, produced by lipophilic phycotoxins: an overview. Rev. Gal. Recur. Mariños (Monogr.) 1, 1–70. Google Scholar
Bligh, E.G., Dyer, W.J., 1959, A rapid method for total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917. CrossRefGoogle Scholar
Dahl E., Yndestad M., 1985, Diarrhetic shellfish poisoning (DSP) in Norway in the autumn 1984 related to the occurence of Dinophysis spp. In: Anderson D., White A., Baden D.G. (Eds), Toxic dinoflagellates. Elsevier Science Publishing, pp. 495–500.
De Zwaan A., Mathieu M., 1992, Cellular biochemistry and endocrinology. In: Goslin, E. (Ed.), The mussel, Mytilus: ecology, physiology, genetics and culture. Elsevier Publishers B.V., Amsterdam, pp. 425–464.
Dubois, F., Gille, X.A., Hamilton, J.K., Rebecs, P.A., Smit, F., 1956, Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350–356. CrossRefGoogle Scholar
Duinker, A., Bergslien, M., Strand, O., Olseng, C.D., Svardal, A., 2007, The effect on size and age on depuration rates of diarrhetic shellfish toxins (DST) in mussels (Mytilus edulis L.). Harmful Algae 6, 288–300. CrossRefGoogle Scholar
Edebo, L., Lange, S., Li, X.P., Allenmark, S., Lindgren, K., Thompson, R., 1988, Seasonal, geographic and individual variation of okadaic acid content in cultivated mussels in Sweden. Acta Pathol. Microbiol. Immunol. Scand. (APMIS) 96, 1036–1042. CrossRefGoogle ScholarPubMed
Fernández, M.L., Míguez, A., Moroño, A., Cacho, E., Martínez, A., Blanco, J., 1998, Detoxification of low polarity toxins (DTX3) from mussels Mytilus galloprovincialis in Spain. In: Reguera B., Blanco J., Fernández M.L, Wyatt T. (Eds), Harmful Algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO.
Fux, E., Marcaillou, C., Mondeguer, F., Bire, R., Hess, P., 2008, Field and mesocosm trials on passive sampling for the study of adsorption and desorption behaviour of lipophilic toxins with a focus on OA and DTX1. Harmful Algae 7, 574–583. CrossRefGoogle Scholar
Haamer, J., Andersson, P.O., Lange, S., Li, X.P., Edebo, L., 1990, Effects of transplantation and reimmersion of mussels Mytilus edulis Linnaeus, 1728, on their contents of okadaic acid. J. Shellfish Res. 9, 109–112. Google Scholar
Hu, T., Doyle, J., Jackson, D., Marr, J., Nixon, E., Pleasance, S., Quilliam, M., Walter, J., Wright, J., 1992a, Isolation of a new diarrhetic shellfish from Irish mussels. J. Chem. Soc. 30, 39–41. Google Scholar
Hu, T., Marr, J., de Freitas, A.S.W., Quilliam, M.A., Walter, J.A., Wright, J.L.C., Pleasance, S., 1992b, New diol esters of okadaic acid isolated from cultures of the dinoflagellates Prorocentrum lima and Prorocentrum concavum . J. Nat. Products 55, 1631–1637. CrossRefGoogle Scholar
Lindahl O., Hageltorn M., 1986, Detoxification experiment of DSP in blue mussels. In: Proc. 4th Nordic Veterinary Congress, Stockholm, pp. 463–466.
Lorenzen C.J., Jeffrey S.W., 1980, Determination of chlorophyll in seawater. UNESCO, Technical Paper in Marine Science N° 35.
MacKenzie, L., Beuzenberg, V., Holland, P., McNabb, P., Selwood, A., 2004, Solid Phase Adsorption Toxin Tracking (SPATT): a new monitoring tool that simulates the biotoxin contamination of filter feeding bivalves. Toxicon 44, 901–918. CrossRefGoogle ScholarPubMed
Marcaillou-Le Baut C., Bardin B., Bardouil M., Bohec M., Le Dean L., Masselin P., Truquet P., 1993, DSP depuration rates of mussels reared in a laboratory and an aquaculture pond. In: Smayda T., Shimitzu Y. (Eds), Toxic Phytoplankton Blooms in the sea. Elsevier, Amsterdam, pp. 531–536.
Marcaillou, C., Mondeguer, F., Gentien, P., 2005, Contribution to toxicity assessment of Dinophysis acuminata (Dinophyceae). J. Appl. Phycol. 17, 155–160. CrossRefGoogle Scholar
Marr, J.C., Hu, T., Pleasance, S., Quilliam, M.A., Wright, J.L.C., 1992, Detection of new 7-O-acyl derivatives of diarrhetic shellfish poisoning toxins by liquid chromatography-mass spectrometry. Toxicon 30, 1621–30. CrossRefGoogle ScholarPubMed
Miles, C.O., Wilkins, A.L, Munday, R., Dines, M.H., Hawkes, A.D., Briggs, L.R., Sandvik, M., Jensen, D.J., Cooney, J.M., Holland, P.T., Quilliam, M.A., MacKenzie, A.L., Beuzenberg, V., Towers, N.R., 2004, Isolation of pectenotoxin-2 from Dinophysis acuta and its conversion to pectenotoxin-2 seco acid, and preliminary assessment of their acute toxicities. Toxicon 43, 1–9. CrossRefGoogle ScholarPubMed
Miles, C.O., Wilkins, A.L., Hawkes, A.D., Jensen, D.J., Cooney, J.M., Larsen, K., Petersen, D., Rise, F., Beuzenberg, V., MacKenzie, A.L., 2006, Isolation and identification of a cis-C8-diol-ester of okadaic acid from Dinophysis acuta in New Zealand. Toxicon 48, 195–203. CrossRefGoogle Scholar
Mondeguer F., Rouland C., Mestres G., 2003, Validation d’un procédé automatisé d’extraction sur phase solide de glande digestive de moule pour l’identification et la quantification des Dinophysis toxines en LC/ESI/MS2 par piégeage d’ions quadripolaire. Rapp. Scient. Techn. Ifremer/ISTPM DEL/03.01 PN.
Mondeguer F., Genin E., Mestre G., Nsengiyumva C., 2004, Validation of an automated procedure of solid phase extraction of mussel digestive glands for identification and quantification of Dinophysis toxins in LC/ESI/MS2 by quadrupole ion trap. In: Proc. 5th International Conference on Molluscan Shellfish Safety, Galway, 14-18 June 2004, pp. 94–99.
Moroño, A., Arévalo, F., Fernández, M.L., Maneiro, J., Pazos, Y., Salgado, C., Blanco, J., 2003. Accumulation and transformation of DSP toxins in mussels Mytilus galloprovincialis during a toxic episode caused by Dinophysis acuminata . Aquat. Toxicol. 62, 269–280. CrossRefGoogle ScholarPubMed
Murata, M., Shimatani, M., Sugitani, H., Oshima, Y., Yasumoto, T., 1982, Isolation and structural elucidation of the causative toxin of diarrhetic shellfish poisoning. Bull. Jpn. Soc. Sci. Fish. 48, 549–552. CrossRefGoogle Scholar
Poletti R., Viviani R., Casadei C., Lucentini L., Giannetti L., Funari E., Draisci R., 1996, Decontamination dynamics of mussels naturally contaminated with diarrhetic toxins relocated to a basin of the Adriatic Sea. In: Yasumoto T., Oshima Y., Fukuyo Y.(Eds.), Harmful and toxic algal blooms. Int. Oceanogr. Comm. UNESCO, pp. 429–432.
Quilliam M.A., Hardstaff W.R., Ishida N., McLachlan J.L., Reeves A.R., Rose N.W., Windust A.J., 1996, Production of diarrhetic shellfish poisoning (DSP) toxins by Prorocentrum lima in culture and development of analytical methods. In: Yasumoto T., Oshima Y., Fukuyo Y. (Eds.), Harmful and Toxic Algal Blooms, 7th International Conference on Toxic Phytoplankton. Int. Oceanogr. Comm. UNESCO, Senday, pp. 289–292.
Sidari, L., Nichetto, P., Cok, S., Sosa, S., Tubaro, A., Honsell, G., Della Logia, R., 1998, Phytoplankton selection by mussels, and diarrhetic shellfish poisoning. Mar. Biol. 131, 103–111. CrossRefGoogle Scholar
Suzuki, S., Otab, H., Yamasaki, M., 1999, Direct evidence of transformation of dinophysistoxin-1 to 7-O-acyl-dinophysistoxin-1 (dinophysistoxin-3) in the scallop Pactinopecten yessoensis . Toxicon 37, 187–198. CrossRefGoogle Scholar
Suzuki, S., Mitsuya, T., 2001, Comparison of dinophysistoxin-1 and esterified dinophysistoxin-1 (dinophysistoxin-3) contents in the scallop Patinopecten yessoensis and the mussel Mytilus galloprovincialis . Toxicon 39, 905–908. CrossRefGoogle Scholar
Suzuki, T., Beuzenberg, V., Mackenzie, L., Quilliam, M.A., 2004, Discovery of okadaic esters in the toxic dinoflagellate Dinophysis acuta from New Zealand using liquid chromatography/tandem mass spectrometry. Rapid Comm. Mass Spectrom. 18, 1131–1138. CrossRefGoogle ScholarPubMed
Suzuki, T., Igarashi, T., Ichimi, K., Watai, M., Suzuki, M., Ogiso, E., Yasumoto, T., 2005, Kinetics of diarrhetic shellfish poisoning toxins, okadaic acid, dinophysistoxin-1, pectenotoxin-6 and yessotoxin in scallops Patinopecten yessoensis . Fish. Sci. 71, 948–955. CrossRefGoogle Scholar
Svensson, S., 2003, Depuration of okadaic acid (diarrhetic toxin) in mussels, Mytilus edulis (Linnaeus), feeding on different quantities of non-toxic algae. Aquaculture 218, 277–291. CrossRefGoogle Scholar
Svensson, S., Förlin, L., 2004, Analysis of the importance of lipid breakdown for elimination of okadaic acid (diarrhetic shellfish toxin) in mussels, Mytilus edulis: results from a field study and a laboratory experiment. Aquat. Toxicol. 66, 405–418. CrossRefGoogle Scholar
Torgersen, T., Sandvik, M., Lundve, B., Lindegarth, S., 2008, Profiles and levels of fatty acid esters of okadaic acid group toxins and pectenotoxins during toxin depuration. Part II: Blue mussels (Mytilus edulis) and flat oyster (Ostrea edulis). Toxicon 52, 418–427. CrossRefGoogle Scholar
Vale, P., Sampayo, M.A., 2002, Esterification of DSP toxins by Portuguese bivalves from the Northwest coast determined by LC-MS a widespread phenomenon. Toxicon 40, 33–42. CrossRefGoogle ScholarPubMed
Yanagi, T., Murata, M., Torigoe, K., Yasumoto, T., 1989, Biological activities of semisynthetic analogs of dinophysistoxin-3, the major diarrhetic shellfish toxin. Agric. Biol. Chem. 53, 525–529. Google Scholar
Yasumoto, T., Oshima, Y., Yamaguchi, M., 1978, Occurrence of a new type of shellfish poisoning in the Tohoku district. Bull. Jpn. Soc. Sci.. Fish. 44, 1249–1255. CrossRefGoogle Scholar
Yasumoto, T., Murata, M., Oshima, Y., Sano, M., Matsumoto, G.K., Clardy, J., 1985, Diarrhetic shellfish toxins. Tetrahedron 41, 1019–1025. CrossRefGoogle Scholar