Scientia Marina, Vol 71, No 2 (2007)

Bioaccumulation and biochemical responses in mussels exposed to the water-accommodated fraction of the Prestige fuel oil

Montserrat Solé, Astrid Buet, Laura Ortiz, Francesc Maynou, Josep Maria Bayona, Joan Albaigés



The activity of the antioxidant defences catalase (CAT, EC, glutathione peroxidase (t-GPX, EC, glutathione reductase (GR, EC, phase II glutathione S-transferase (GST, EC along with the NADPH-dependent cytochrome c (CYP) reductase (EC, NADH-dependent cytochrome c reductase (EC, and NADH-dependent ferricyanide (b5) reductase (EC was determined in the digestive gland of mussels Mytilus galloprovincialis fed with Tetraselmis sp. pre-exposed to the water accommodated fraction of the Prestige oil. Mussel gills were also used for measuring acetylcholinesterase activity (AChE, EC and lipid peroxidation (LP) as an indication of neurotoxicity and oxidative stress damage respectively. Bioaccumulation of the selected polycyclic aromatic hydrocarbons (2 to 6 rings PAHs) in mussels after 2, 4, 7 and 10 days of exposure did not show any significant trend; the 2-3 ring PAHs were best represented (51%). A significant (p<0.05) bioaccumulation in exposed mussels was only observed for some alkylated 2-3 ring PAHs. Biochemical antioxidant responses (CAT, t-GPX and GR) significantly increased over time, regardless of exposure, whereas NADH-dependent reductases and LP were affected, regardless of the length of exposure. However, due to the low solubility of the Prestige crude, the PAH levels reached in exposed mussels were not sufficient to cause a clearly associated biochemical response.


Prestige oil spill; Mytilus galloprovincialis; Tetraselmis sp.; water-accommodated fraction; biomarkers

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Akcha, F., C., Izuel, P., Venier, H., Budzinski, T. Burgeot and J-F. Narbonne. – 2000. Enzymatic biomarker measurement and study of DNA adduct formation in benzo(a)pyrene-contaminated mussels, Mytilus galloprovincialis. Aquat. Toxicol., 49: 269-287. doi:10.1016/S0166-445X(99)00082-X PMid:10854671

Albaigés, J. and J.M. Bayona. – 2003. El Fuel. In: S.R. Fernández- Latorre (ed.), La Huella del Fuel. Ensayos Sobre el Prestige, pp. 80-103. Fundación Santiago Rey Fernández-Latorre, A Coruña.

Albers, P.H. – 2003. Petroleum and individual polycyclyc aromatic hydrocarbons. In: D.J. Hoffman, B.A. Rattner, G.A. Burton, J. Cairns (eds), Handbook of Ecotoxicology, pp.1-32. Lewis Publishers, New York.

Barata, C., A. Calbet, E. Saiz, L. Ortiz and J.M. Bayona. – 2005. Predicting single and mixture toxicity of petrogenic polycyclic aromatic hydrocarbons to the copepod Oithona davisae. Environ. Toxicol. Chem., 24: 2992-2999. doi:10.1897/05-189R.1 PMid:16398138

Baumard, P., H. Budzinski, P. Garrigues, J.C. Sorbe, T. Burgeot and J. Belloco. – 1998. Concentrations of PAHs (Polycyclic aromatic hydrocarbons) in various marine organisms in relation to those in sediment and to trophic level. Mar. Pollut. Bull., 36: 951-960. doi:10.1016/S0025-326X(98)00088-5

Bodin, N., T. Burgeot, J.Y. Stanisière, G. Bocquené, D. Menard, C. Minier, I. Boutet, A. Amat, Y. Cherel and H. Budzinski. – 2004. Seasonal variations of a battery of biomarkers and physiological indices for the mussel Mytilus galloprovincialis transplanted into the northwest Mediterranean Sea. Comp. Biochem. Physiol., 138C: 411-427.

Bradford, M. – 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem., 72: 248-254. doi:10.1016/0003-2697(76)90527-3 PMid:942051

Cajaraville, M.P., J.A. Uranga and E. Angulo. – 1992. Comparative effects of the water acommodated fraction of three oil son mussels- 3. Quantitative histochemistry of enzymes related to the detoxication metabolism. Comp. Biochem. Physiol., 103C: 369-377.

Canova, S., P. Degan, L.D. Peters, D.R. Livingstone, R. Voltan and P. Venier. – 1998. Tissue dose, DNA adducts, oxidative DNA damage and CYP1A-immunopositive proteins in mussels exposed to waterborne benzo(a)pyrene. Mutation Res., 399: 17-30. doi:10.1016/S0027-5107(97)00263-7

Carlberg, I. and B. Mannervik. – 1985. Glutathione reductase. Methods Enzymol., 113: 485-490.

Cheung, C.C.C., W.H.L. Siu, B.J. Richardson, S.B. De Luca- Abbott and P.K.S. Lam. – 2004. Antioxidant responses to benzo(a)pyrene and Arochlor 1254 exposure in the greenlipped mussel, Perna viridis. Environ. Pollut., 128: 393-403. doi:10.1016/j.envpol.2003.09.010 PMid:14720481

D’Adamo, R., S. Pelosi, P. Trotta and G. Sansone. – 1997. Bioaccumulation and biomagnification of polycyclic aromatic hydrocarbons in aquatic organisms. Mar. Chem., 56: 45-49. doi:10.1016/S0304-4203(96)00042-4

Durand, F., L.D. Peters and D.R. Livingstone. – 2002. Effect of intertidal compared to subtidal exposure on the uptake, loss and oxidative toxicity of water-born benzo(a)pyrene in the mantle and whole tissues of the mussel, Mytilus edulis L. Mar. Environ. Res., 54: 271-274. doi:10.1016/S0141-1136(02)00199-X PMid:12408575

Ellman, G.L., K.O. Courtney, V. Andrers Jr and R.M. Featherstone. – 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol., 7: 88-95. doi:10.1016/0006-2952(61)90145-9 PMid:13726518

Fitzpatrick, P.J., J. O’Halloran, D. Sheehan and A.R. Walsh. – 1997. Assessment of the glutathione S-transferase and related proteins in the gill and digestive gland of Mytilus edulis (L.) as potential organic pollution biomarkers. Biomarkers, 2: 51-56. doi:10.1080/135475097231977

Gowland, B., A. McIntosh, I. Davies, C. Moffat and L. Webster. – 2002. Implications from a field study regarding the relationship between polycyclic aromatic hydrocarbons and glutathione Stransferase activity in mussels. Mar. Environ. Res., 54: 231-235. doi:10.1016/S0141-1136(02)00129-0 PMid:12408567

Hamountene, D., J.F. Payne, A. Rahimtula and K. Lee. – 2002. The use of the Comet assay to assess DNA damage in hemocytes and digestive gland cells of mussels and clams exposed to water contaminated with petroleum hydrocarbons. Mar. Environ. Res., 54: 471-474. doi:10.1016/S0141-1136(02)00162-9 PMid:12408603

Krishnakumar, P.K., E. Casillas and U. Varanasi. – 1997. Cytochemical responses in the digestive tissue of Mytilus edulis complex exposed to microencapsulated PAHs or PCBs. Comp. Biochem. Physiol., 118C: 11-18.

Labarta, U., M.J. Fernández-Reiriz, J.L. Garrido, J.M.F. Babarro, J.M. Bayona and Albaigés, J. – 2005. Response of mussel recruits to pollution from the “Prestige” oil spill along the Galicia coast. A biochemical approach. Mar. Ecol. Prog. Ser., 302: 135-145. doi:10.3354/meps302135

Livingstone, D.R. – 1987. Seasonal responses to diesel oil and subsequent recovery of the cytochrome P-450 monooxygenase system in the common mussel, Mytilus edulis L., and the periwinkle, Littorina littorea L. Sci. Total Environ., 65: 3-20. doi:10.1016/0048-9697(87)90157-4

Livingstone, D.R. – 2001. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar. Pollut. Bull., 42: 656-666. doi:10.1016/S0025-326X(01)00060-1 PMid:11525283

Marigómez, I., M. Soto, I. Cancio, A. Orbea, L. Garmendia and M.P. Cajaraville. – 2006. Cell and tissue biomarkers in mussel, and histopathology in hake and anchovy from Bay of Biscay alter the Prestige oil spill (Monitoring campaign 2003). Mar. Pollut. Bull., 53: 287-304. doi:10.1016/j.marpolbul.2005.09.026 PMid:16271373

Michel, X.R., P. Suteau, L.W. Robertson and J.-F. Narbonne. – 1993. Effects of benzo(a)pyrene, 3,3’,4,4’-tetrachlorobiphenyl and 2,2’,4,4’,5,5’-hexachlorobiphenyl on the xenobioticmetabolizing enzymes in the mussel (Mytilus galloprovincialis). Aquat. Toxicol., 27: 3535-344. doi:10.1016/0166-445X(93)90062-6

Moreira, S.M., M. Moreira-Santos, R. Ribeiro and L. Guilhermino. – 2004. The “Coral Bulker” fuel oil spill on the North Coast of Portugal: Spatial and Temporal biomarker responses in Mytilus galloprovincialis. Ecotoxicology, 13: 619-630. doi:10.1007/s10646-003-4422-3 PMid:15673211

Navas, J.M., M. Babín, S. Casado, C. Fernández and J.V. Tarazona. – 2006. The Prestige oil spill: A laboratory study about the toxicity of the water-soluble fraction of the fuel oil, Mar. Environ. Res., 62: S352-S355. doi:10.1016/j.marenvres.2006.04.026 PMid:16709428

Okay, O.S., P. Donkin, L.D. Peters and D.R. Livingstone. – 2000. The role of algae (Isochrysis galvana) enrichment on the bioaccumulation of benzo(a)pyrene and its effects on the blue mussel Mytilus edulis. Environ. Pollut., 110: 103-113. doi:10.1016/S0269-7491(99)00282-1 PMid:15092860

Pérez-Cadahía, B., B. Laffon, E. Pásaro and J. Méndez. – 2004. Evaluation of PAH bioaccumulation and DNA damage in mussels (Mytilus galloprovincialis) exposed to spilled Prestige crude oil. Comp. Biochem. Physiol., 138C: 453-460.

Porte, C., X. Biosca, M. Solé and J. Albaigés. – 2000. The Aegean Sea oil spill on the Galician coast (NW Spain). III. The assessment of long-term sublethal effects on mussels. Biomarkers, 5: 436-446. doi:10.1080/135475000750052448

Porte, C., X. Biosca, M. Solé and J. Albaigés. – 2001a. The integrated use of chemical analysis, cytochrome P450 and stress proteins in mussels to assess pollution along the Galician coast (NW Spain). Environ. Pollut., 112: 261-268. doi:10.1016/S0269-7491(00)00104-4 PMid:11234544

Porte, C., M. Solé, V. Borghi, M. Martínez, J. Chamorro, A. Torreblanca, M. Ortiz, A. Orbea, M. Soto and M.P. Cajaraville. – 2001b. Chemical, biochemical and cellular responses in the digestive gland of the mussel Mytilus galloprovincialis from the Spanish Mediterranean Coast. Biomarkers, 6: 335-350. doi:10.1080/13547500110044771

Seruto, C., Y. Sapozhnikova and D. Schlenk. – 2005. Evaluation of the relationship between biochemical endpoints of PAHs exposure and physiological endpoints of reproduction in male California Halibut (Paralichthys californicus) exposed to sediments from a natural oil seep. Mar. Environ. Res., 60: 454-465. doi:10.1016/j.marenvres.2005.01.004 PMid:15924994

Singer, M.M., D. Aurand, G.E. Bragins, J.R. Clark, G.M. Coelho, M.L. Sowby and R.S. Tjeerdema. – 2000. Standarization of the Preparation and Quantification of water-accommodated fractions of petroleum for toxicity testing. Mar. Pollut. Bull., 40: 1007-1016. doi:10.1016/S0025-326X(00)00045-X

Sokal, R.R. and F.J. Rohlf. – 1981. Biometry. Freeman and Co, San Francisco.

Solé, M. and D.R. Livingstone. – 2005. Components of the cytochrome P450-dependent monooxygenase system and ‘NADPH-independent benzo[a]pyrene hydroxylase’ activity in a wide range of marine invertebrate species. Comp. Biochem. Physiol., 141C: 20-31.

Solé, M., C. Porte, X. Biosca, C.L. Mitchelmore, J.K. Chipman, D.R. Livingstone and J. Albaigés. – 1996. Effects of the “Aegean Sea” oil spill on biotransformation enzymes, oxidative stress and DNA-adducts in digestive gland of the mussel (Mytilus edulis.L.). Comp. Biochem. Physiol., 113C: 257-265.

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