Cellular and biochemical responses of the oyster Crassostrea gigas to controlled exposures to metals and Alexandrium minutum

Aquatic Toxicology

Volumn 147, Issue , 2014, Pages 158-167

  Haberkorn, Hansy ^a   Lambert, Christophe ^a   Le Goïc, Nelly ^a   Quéré, Claudie ^b   Bruneau, Audrey ^a   Riso, Ricardo ^a   Auffret, Michel ^a   Soudant, Philippe ^a  

^a INSTITUT UNIVERSITAIRE EUROPÉEN DE LA MER   (France)

^b IFREMER   (France)

Author keywords

Harmful algae; Metals; Oysters; Physiological effects; Toxin accumulation

Indexed keywords

ACYLGLYCEROL; CADMIUM; CARDIOLIPIN; CERAMIDE; CERAMIDEAMINOETHYLPHOSPHONATE; COPPER; DIACYLGLYCEROL; ETHER GLYCERIDE; MONOACYLGLYCEROL; MONOPHENOL MONOOXYGENASE; PARALYTIC SHELLFISH TOXIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; REACTIVE OXYGEN METABOLITE; SHELLFISH TOXIN; STEROL; UNCLASSIFIED DRUG;

ALGA; BIOACCUMULATION; BIVALVE; DINOFLAGELLATE; HEAVY METAL; PHYSIOLOGICAL RESPONSE; TOXICITY; TOXIN;

ALEXANDRIUM MINUTUM; ALGA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BLOOD CELL; CELL DEATH; CONTROLLED STUDY; CRASSOSTREA GIGAS; DINOFLAGELLATE; EXOCRINE GLAND; LIPID COMPOSITION; LIPID METABOLISM; LIPID PEROXIDATION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; TISOCHRYSIS LUTEA;

HARMFUL ALGAE; METALS; OYSTERS; PHYSIOLOGICAL EFFECTS; TOXIN ACCUMULATION;

ANIMALS; CADMIUM; COPPER; CRASSOSTREA; DINOFLAGELLIDA; HEMOCYTES; MARINE TOXINS; PHAGOCYTOSIS; WATER POLLUTANTS, CHEMICAL;

EID: 84892188772     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.12.012     Document Type: Article

References (72)

1. Abbe G.R., Riedel G.F., Sanders J.G. Factors that influence the accumulation of copper and cadmium by transplanted eastern oysters (Crassostrea virginica) in the Patuxent River, Maryland. Mar. Environ. Res. 2000, 49:377-396.
2. Arzul G., Seguel M., Guzman L., Erard-Le Denn E. Comparison of allelopathic properties in three toxic Alexandrium species. J. Exp. Mar. Biol. Ecol. 1999, 232:285-295.
3. Auffret M., Oubella R. Cytological and cytometric analysis of bivalve mollusc hemocytes. Tech. Fish Immunol. 1995, 4:55-63.
4. Auffret M., Mujdzic N., Corporeau C., Moraga D. Xenobiotic-induced immunomodulation in the European flat oyster, Ostrea edulis. Mar. Environ. Res. 2002, 54:585-589.
5. Baars A.J., Theelen R.M.C., Janssen P.J.C.M., Hesse J.M., van Apeldoorn M.E., Meijerink M.C.M., Verdam L., Zeilmaker M.J. Re-evaluation of human-toxicological maximum permissible risk levels RIVM. Rijsinstituut voor volksgezondheid en milieu. Report 711 701 025 2001.
6. Baudrimont M., de Montaudouin X. Evidence of altered protective effect of metallothioneins after cadmium exposure in the digenean parasite-infected cockle (Cerastoderma edule). Parasitology 2007, 134:237-245.
7. Bouilly K., Gagnaire B., Bonnard M., Thomas-Guyon H., Renault T., Miramand P., Lapègue S. Effects of cadmium on aneuploidy and hemocyte parameters in the Pacific oyster Crassostrea gigas. Aquat. Toxicol. 2006, 78:149-156.
8. Bricelj V.M., Shumway S.E. Paralytic Shellfish Toxins in bivalve molluscs: occurrence, transfer kinetics, and biotransformation. Res. Fish. Sci. 1998, 6:315-383.
9. Cheng T.C. In vivo effects of heavy metals on cellular defense mechanisms of Crassostrea virginica: total and differential cell counts. J. Invertebr. Pathol. 1988, 51:207-214.
10. Cheng T.C. Effects of In Vivo Exposure of Crassostrea virginica to Heavy Metals on Hemocyte Viability and Activity Levels of Lysosomal Enzymes 1990, Academic Press, San Diego, CA, USA.
11. Cherkasov A.S., Grewal S., Sokolova I.M. Combined effects of temperature and cadmium exposure on haemocyte apoptosis and cadmium accumulation in the eastern oyster Crassostrea virginica (Gmelin). J. Therm. Biol. 2007, 32:162-170.
12. Chora S., Starita-Geribaldi M., Guigonis J.M., Samson M., Roméo M., Bebianno M.J. Effect of cadmium in the clam Ruditapes decussatus assessed by proteomic analysis. Aquat. Toxicol. 2009, 94:300-308.
13. Chu F.L.E., Soudant P., Hale R.C. Relationship between PCB accumulation and reproductive output in conditioned oysters Crassostrea virginica fed a contaminated algal diet. Aquat. Toxicol. 2003, 65:293-307.
14. Da Silva P.M., Hégaret H., Lambert C., Wikfors G.H., Le Goïc N., Shumway S.E., Soudant P. Immunological responses of the Manila clam (Ruditapes philippinarum) with varying parasite (Perkinsus olseni) burden, during a long-term exposure to the harmful alga, Karenia selliformis, and possible interactions. Mar. Pollut. Bull. 2008, 50:733-739.
15. + exchanger in the induction of cadmium toxic effects. Fish Shellfish Immunol. 2009, 27:446-453.
16. Delaporte M., Soudant P., Moal J., Lambert C., Quéré C., Miner P., Choquet G., Paillard C., Samain J.F. Effect of a mono-specific algal diet on immune functions in two bivalve species - Crassostrea gigas and Ruditapes philippinarum. J. Exp. Biol. 2003, 206:3053-3064.
17. Donaghy L., Lambert C., Choi K-S., Soudant P. Hemocytes of the carpet shell clam (Ruditapes decussatus) and the Manila clam (Ruditapes philippinarum): current knowledge and future prospects. Aquaculture 2009, 297:10-24.
18. Dorsey A., Ingerman L., Swarts S. Toxicological Profile for Copper 2004, 314. Agency for Toxic Substances and Disease Registry, United States.
19. Emura A., Matsuyama Y., Oda T. Evidence for the production of a novel proteinaceous hemolytic exotoxin by dinoflagellate Alexandrium taylori. Harmful Algae 2004, 3:29-37.
20. Evans D.W., Irwin S.W.B., Fitzpatrick S. The effect of digenean (Platyhelminthes) infections on heavy metal concentrations in Littorina littorea. J. Mar. Biol. Assoc. U.K. 2001, 81:349-350.
21. Evrard E., Devaux A., Bony S., Burgeot T., Riso R., Budzinski H., Le Du M., Quiniou L., Laroche J. Responses of the European flounder Platichthys flesus to the chemical stress in estuaries: load of contaminants, gene expression, cellular impact and growth rate. Biomarkers 2010, 15(2):111-127.
22. Faroon O., Ashizawa A., Wright S., Tucker P., Jenkins K., Ingerman L., Rudisill C. Toxicological Profile for Cadmium. Agency for Toxic Substances and Disease Registry 2012, U.S. Department of Health and Human Services, Public Health Service, Atlanta, GA, 487 p.
23. Ford S.E., Bricelj V.M., Lambert C., Paillard C. Deleterious effects of a nonPST bioactive compound(s) from Alexandrium tamarense on bivalve hemocytes. Mar. Biol. 2008, 154:241-253.
24. Gagné F., Auclair J., Turcotte P., Fournier M., Gagnon C., Sauvé S., Blaise C. Ecotoxicity of CdTe quantum dots to freshwater mussels: impacts on immune system, oxidative stress and genotoxicity. Aquat. Toxicol. 2008, 86:333-340.
25. Galimany E., Sunila I., Hégaret H., Ramón M., Wikfors G.H. Experimental exposure of the blue mussel (Mytilus edulis L.) to the toxic dinoflagellate Alexandrium fundyense: histopathology, immune responses, and recovery. Harmful Algae 2008, 7:702-711.
26. Galimany E., Sunila I., Hégaret H., Ramón M., Wikfors G.H. Pathology and immune response of the blue mussel (Mytilus edulis L.) after an exposure to the harmful dinoflagellate Prorocentrum minimum. Harmful Algae 2008, 7:630-638.
27. Galimany E., Place A.R., Ramón M., Jutson M., Pipe R.K. The effects of feeding Karlodinium veneficum (PLY # 103; Gymnodinium veneficum Ballantine) to the blue mussel Mytilus edulis. Harmful Algae 2008, 7:91-98.
28. Géret F., Jouan A., Turpin V., Bebianno M.J., Cosson R.P. Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalve mollusks: the oyster (Crassostrea gigas) and the mussel (Mytilus edulis). Aquat. Living Resour. 2002, 15:61-66.
29. Guillard R.R.L., Hargraves P.E. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 1993, 32:234-236.
30. Haberkorn H. Impact du dinoflagellé toxique, Alexandrium minutum, sur l'huître creuse, Crassostrea gigas: approche intégrative 2009, 174. (Thesis), Université de Bretagne Occidentale.
31. Haberkorn H., Lambert C., Le Goïc N., Guéguen M., Moal J., Palacios E., Lassus P., Soudant P. Effects of Alexandrium minutum exposure on physiological and hematological variables of diploid and triploid oysters, Crassostrea gigas. Aquat. Toxicol. 2010, 97:96-108.
32. Haberkorn H., Lambert C., Le Goïc N., Moal J., Suquet M., Guéguen M., Sunila I., Soudant P. Effects of Alexandrium minutum exposure on nutrition-related processes and reproductive output in oysters Crassostrea gigas. Harmful Algae 2010, 9:427-439.
33. Haberkorn H., Tran D., Massabuau J-C., Ciret V., Savar P., Soudant P. Relationship between valve activity, microalgae concentration in the water and toxin accumulation in the digestive gland of the Pacific oyster, Crassostrea gigas, exposed to Alexandrium minutum. Mar. Pollut. Bull. 2011, 62:1191-1197.
34. Hégaret H., Wikfors G., Soudant P., Lambert C., Shumway S., Bérard J., Lassus P. Toxic dinoflagellates (Alexandrium fundyense and A. catenella) have minimal apparent effects on oyster hemocytes. Mar. Biol. 2007, 152:441-447.
35. Hégaret H., da Silva P.M., Wikfors G.H., Lambert C., De Bettignies T., Shumway S.E., Soudant P. Hemocyte responses of Manila clams, Ruditapes philippinarum, with varying parasite, Perkinsus olseni, severity to toxic-algal exposures. Aquat. Toxicol. 2007, 84:469-479.
36. Huss H.H. Aquatic biotoxins. Assessment and Management of Seafood Safety and Quality. FAO Fisheries Technical Paper 2003, (Chapter 5.1.5), p. 239. H.H. Huss, L. Ababouch, L. Gram (Eds.).
37. International Agency for Research on Cancer (IARC) Cadmium and Cadmium Compounds 1993, vol. 58:119.
38. Lambert C., Soudant P., Choquet G., Paillard C. Measurement of Crassostrea gigas hemocyte oxidative metabolism by flow cytometry and the inhibiting capacity of pathogenic vibrios. Fish Shellfish Immunol. 2003, 15:225-240.
39. Landsberg J.H. The effects of harmful algal blooms on aquatic organisms. Fish. Sci. 2002, 10:113-390.
40. Lassus P., Bardouil M., Ledoux M., Murail I., Bohec M., Truquet P., Frémy J.-M., Rohmer V. Paralytic phycotoxin uptake by scallops (Pecten maximus). Aquat. Living Resour. 1992, 5:319-324.
41. Lelong A., Haberkorn H., Le Goïc N., Hégaret H., Soudant P. A new insight into allelopathic effects of Alexandrium minutum on photosynthesis and respiration of the diatom chaetoceros neogracile revealed by photosynthetic-performance analysis and flow cytometry. Microb. Ecol. 2011, 62(4):919-930.
42. Le Moine S., Sellos D., Moal J., Daniel J.Y., San Juan S.F., Samain J.F., Van Wormhoudt A. Amylase on Pecten maximus (mollusca, bivalves): protein and cdna characterization; quantification of the expression in the digestive gland. Mol. Mar. Biol. Biotechnol. 1997, 6:228-237.
43. Lekhi P., Cassis D., Pearce C.M., Ebell N., Maldonado M.T., Orians K.J. Role of dissolved and particulate cadmium in the accumulation of cadmium in cultured oysters (Crassostrea gigas). Sci. Total Environ. 2008, 393:309-325.
44. Lin W., Rice M.A., Chien P.K. The effects of copper, cadmium and zinc on particle filtration and uptake of glycine in the pacific oyster Crassostrea gigas. Comp. Biochem. Physiol. C Comp. Pharmacol. 1992, 103:181-187.
45. Lin W., Rice M.A., Chien P.K. The differential effects of three heavy metals on particle filtration and amino acid uptake by the Pacific oyster, Crassostrea gigas. J. Shellfish Res. 1993, 12:111.
46. Marie D., Partensky F., Vaulot D., Brussaard C. Enumeration of phytoplankton, bacteria, and viruses in marine samples. Curr. Protoc. Cytom. 1999, 11.11.11-11.11.15. John Wiley & Sons Inc., New York.
47. Morley N.J. Interactive effects of infectious diseases and pollution in aquatic mollusks. Aquat. Toxicol. 2010, 96:27-36.
48. Mouneyrac C., Amiard J.C., Amiard-Triquet C. Effects of natural factors (salinity and body weight) on cadmium, copper, zinc and metallothionein-like protein levels in resident populations of oysters Crassostrea gigas from a polluted estuary. Mar. Ecol. Prog. Ser. 1998, 162:125-135.
49. Narahashi T. Mechanism of tetrodotoxin and saxitoxin action. Handbook of Natural Toxins. Marine Toxins and Venoms 1988, vol. 3:185-210. Marcel Dekker Inc., New York.
50. O'Connor T.P., Lauenstein G.G. Status and trends of copper concentrations in mussels and oysters in the USA. Mar. Chem. 2005, 97:49-59.
51. Oshima Y. Postcolumn derivatization liquid chromatographic method for paralytic shellfish toxins. J. AOAC Int. 1995, 78:528-532.
52. Parry H.E., Pipe R.K. Interactive effects of temperature and copper on immunocompetence and disease susceptibility in mussels (Mytilus edulis). Aquat. Toxicol. 2004, 69:311-325.
53. Paul-Pont I., Gonzalez P., Baudrimont M., Jude F., Raymond N., Bourrasseau L., Le Goïc N., Haynes F., Legeay A., Paillard C., de Montaudouin X. Interactive effects of metal contamination and pathogenic organisms on the marine bivalve Cerastoderma edule. Mar. Pollut. Bull. 2010, 60:515-525.
54. Pipe R.K., Coles J.A. Environmental contaminants influencing immune function in marine bivalve molluscs. Fish Shellfish Immunol. 1995, 5:581-595.
55. Pipe R.K., Coles J.A., Carissan F.M.M., Ramanathan K. Copper induced immunomodulation in the marine mussel, Mytilus edulis. Aquat. Toxicol. 1999, 46:43-54.
56. Reid H.I., Soudant P., Lambert C., Paillard C., Birkbeck T.H. Salinity effects on immune parameters of Ruditapes philippinarum challenged with Vibrio tapetis. Dis. Aquat. Org. 2003, 56:249-258.
57. Réseau d'Observation de la Contamination Chimique du milieu marin (ROCCH/RNO). Institut français de recherche pour l'exploitation de la mer (IFREMER). http://wwz.ifremer.fr/envlit/surveillance/contaminants_chimiques.
58. Ringwood A.H., Conners D.E., DiNovo A. The effects of copper exposures on cellular responses in oysters. Mar. Environ. Res. 1998, 46:591-595.
59. Riso R.D., Monbet P., Corre P.L. Measurement of copper in sea-water by constant current stripping analysis (CCSA) with a rotating gold disk electrode. Analyst 1997, 122(12):1593-1596.
60. Riso R.D., Le Corre P., Chaumery C.J. Rapid and simultaneous analysis of trace metals (Cu, Pb and Cd) in seawater by potentiometric stripping analysis. Anal. Chim. Acta 1997, 351(1-3):83-89.
61. Roesijadi G. Environmental factors: response to metals. The eastern oyster Crassostrea virginica 1996, 515-537. A Maryland Sea Grant Book, College Park Maryland. V.S. Kennedy, R.I.E. Newell, A.F. Eble (Eds.).
62. Samain J.F., Daniel J.Y., Le Coz J.R. Trypsine, amylase et protéines du zooplancton: dosage automatique et manuel. J. Exp. Mar. Biol. Ecol. 1977, 29:279-289.
63. Sokolova I.M., Evans S., Hughes F.M. Cadmium-induced apoptosis in oyster hemocytes involves disturbance of cellular energy balance but no mitochondrial permeability transition. J. Exp. Biol. 2004, 207:3369-3380.
64. Sures B. Environmental parasitology. Interactions between parasites and pollutants in the aquatic environment. Parasite 2008, 15(3):434-438.
65. Tanguy A., Boutet I., Riso R., Boudry P., Auffret M., Moraga D. Metallothionein genes in the European flat oyster Ostrea edulis: a potential ecological tool for environmental monitoring?. Mar. Ecol. Prog. Ser. 2003, 257:87-97.
66. Tillmann U., Alpermann T., John U., Cembella A. Allelochemical interactions and short-term effects of the dinoflagellate Alexandrium on selected photoautotrophic and heterotrophic protists. Harmful Algae 2008, 7:52-64.
67. Tran D., Fournier E., Durrieu G., Massabuau J.C. Copper detection in the Asiatic clam Corbicula fluminea: optimum valve closure response. Aquat. Toxicol. 2003, 66:333-343.
68. Tran D., Ciret P., Ciutat A., Durrieu G., Massabuau J.-C. Estimation of potential and limits of bivalve closure response to detect contaminants: application to cadmium. Environ. Toxicol. Chem. 2003, 22:116-122.
69. World Health Organization Guidelines for Drinking-water Quality: First Addendum to Third Edition, Volume 1, Recommendations 2006, World Health Organization. http://www.who.int/water_sanitation_health/dwq/gdwq3/en/.
70. Zaldibar B., Cancio I., Marigomez I. Reversible alterations in epithelial cell turnover in digestive gland of winkles (Littorina littorea) exposed to cadmium and their implications for biomarker measurements. Aquat. Toxicol. 2007, 81:183-196.
71. Zaldibar B., Cancio I., Soto M., Marigomez I. Changes in cell-type composition in digestive gland of slugs and its influence in biomarkers following transplantation between a relatively unpolluted and a chronically metal-polluted site. Environ. Pollut. 2008, 156:367-379.
72. Zorita I., Ortiz-Zarragoitia M., Soto M., Cajaraville M.P. Biomarkers in mussels from a copper site gradient (Visnes, Norway): an integrated biochemical, histochemical and histological study. Aquat. Toxicol. 2006, 78:109-116.