Responses of Pacific oyster Crassostrea gigas populations to abiotic stress in environmentally contrasted estuaries along the Atlantic coast of France

Aquatic Toxicology

Volumn 109, Issue , 2012, Pages 70-79

  David, Elise ^a   Tanguy, Arnaud ^b,c   Riso, Ricardo ^a   Quiniou, Louis ^a   Laroche, Jean ^a   Moraga, Dario ^a  

^a INSTITUT UNIVERSITAIRE EUROPÉEN DE LA MER   (France)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

Crassostrea gigas; Environmental stress; Genetic polymorphism; Heavy metals; Metallothionein; Phenotype genotype coupling

Indexed keywords

MESSENGER RNA; METALLOTHIONEIN;

BIOACCUMULATION; BIOTIC FACTOR; ENVIRONMENTAL STRESS; ESTUARINE ENVIRONMENT; GENOTYPE; HEAVY METAL; INHIBITION; MOLLUSC; PHENOTYPE; POLYMERASE CHAIN REACTION; POLYMORPHISM; RNA;

ABIOTIC STRESS; ALLELE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; CRASSOSTREA GIGAS; DELTA 9 DESATURASE GENE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL STRESS; ENZYME LINKED IMMUNOSORBENT ASSAY; ESTUARY; FRANCE; GENE; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETIC MARKER; GENETIC VARIABILITY; GLUTAMINE SYNTHETASE GENE; METALLOTHIONEIN GENE; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; OYSTER; PHOSPHOGLUCOMUTASE GENE; PRIORITY JOURNAL; PROTEIN DETERMINATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEASONAL VARIATION; SENSITIVITY ANALYSIS; TRANSCRIPTION REGULATION; WATER POLLUTION;

ALLELES; ANIMALS; CRASSOSTREA; ENVIRONMENT; FRANCE; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENOTYPE; METALLOTHIONEIN; METALS, HEAVY; SEASONS; STRESS, PHYSIOLOGICAL; WATER POLLUTANTS, CHEMICAL;

ATLANTIC COAST [EUROPE]; ATLANTIC COAST [FRANCE]; FRANCE;

CRASSOSTREA GIGAS; OSTREIDAE;

EID: 84255195460     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.11.014     Document Type: Article

References (96)

1. Amiard J.C., Amiard-Triquet C., Barka S., Pellerin J., Rainbow P.S. Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat. Toxicol. 2006, 76:160-202.
2. Anderson S., Sadinski W., Shugart L., Brussard P., Depledge M., Ford T., Hose J., Stegeman J., Suk W., Wirgin I., et al. Genetic and molecular ecotoxicology: a research framework. Environ. Health Perspect. 1994, 102(Suppl. 12):3-8.
3. Andrews G.K. Mechanisms of regulation of metallothionein gene expression. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2000, 126:6.
4. Andrews G.K. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem. Pharmacol. 2000, 59:95-104.
5. Barton N.H. Genetic hitchhiking. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2000, 355:1553-1562.
6. Belfiore N.M., Anderson S.L. Effects of contaminants on genetic patterns in aquatic organisms: a review. Mutat. Res.: Rev. Mutat. Res. 2001, 489:97-122.
7. Belkhir N.M., Borsa P., Goudet P., Bonhomme F. GENETIX, logiciel sous Windows pour la génétique des populations. Laboratoire Génome et Populations CNRS UPR 9060 1996, Université de Montpellier II, Montpellier, France.
8. Ben-Shlomo R., Nevo E. Isozyme polymorphism as monitoring of marine environments: the interactive effect of cadmium and mercury pollution on the shrimp, Palaemon elegans. Mar. Pollut. Bull. 1988, 19:314-317.
9. Berrebi P. Hétérogénéité génétique et évolution saisonnière du Flet (Platichtys flesus, Osteichtyes, Pleuronectidae) lors de sa phase lagunaire. Vie Milieu 1992, 42:147-156.
10. Bickham J.W., Sandhu S., Hebert P.D., Chikhi L., Athwal R. Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutat. Res. 2000, 463:33-51.
11. Boutet I., Tanguy A., Auffret M., Riso R., Moraga D. Immunochemical quantification of metallothioneins in marine mollusks: characterization of a metal exposure bioindicator. Environ. Toxicol. Chem. 2002, 21:1009-1014.
12. Boutet I., Tanguy A., Moraga D. Response of the Pacific oyster Crassostrea gigas to hydrocarbon contamination under experimental conditions. Gene 2004, 329:147-157.
13. Campton D.E., Berg C.J., Robison L.M., Glazer R.A. Genetic patchiness among populations of queen conch Strombus gigas in the Florida Keys and Bimini. Fish. Bull. 1992, 90:250-259.
14. Chagnon N.L., Guttman S.I. Differential survivorship of allozyme genotypes in mosquitofish populations exposed to copper or cadmium. Environ. Toxicol. Chem. 1989, 8:319-326.
15. Chausson F., Bridges C.R., Sarradin P.M., Green B.N., Riso R., Caprais J.C., Lallier F.H. Structural and functional properties of hemocyanin from Cyanagraea praedator, a deep-sea hydrothermal vent crab. Proteins: Structure, Function and Genetics 2001, 45:351-359.
16. Chen H.I., Chiu Y.W., Hsu Y.K., Li W.F., Chen Y.C., Chuang H.Y. The association of metallothionein-4 gene polymorphism and renal function in long-term lead-exposed workers. Biol. Trace Elem. Res. 2010, 137:55-62.
17. Chessel, D., Dodélec, S. Thioulouse, J., 1995. ADE Version 4: Hypercard Stacks and Program. Library for the Analysis of Environmental Data. URA CNRS 1451, Université de Lyon I, 69622 Villeurbanne Cedex (available at: ). http://biomserv.univ-lyon1.fr/ade-4.html.
18. Cloern J.E. Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser. 2001, 210:223-253.
19. Damiens G., Mouneyrac C., Quiniou F., His E., Gnassia-Barelli M., Romeo M. Metal bioaccumulation and metallothionein concentrations in larvae of Crassostrea gigas. Environ. Pollut. 2006, 140:492-499.
20. David E., Tanguy A., Pichavant K., Moraga D. Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS J. 2005, 272:5635-5652.
21. David E., Boudry P., Dégremont L., Tanguy A., Quéré N., Samain J.F., Moraga D. Genetic polymorphism of glutamine synthetase and delta-9 desaturase in families of Pacific oyster Crassostrea gigas and susceptibility to summer mortality. J. Exp. Mar. Biol. Ecol. 2007, 349:272-283.
22. Depledge M.H. Genetic ecotoxicology: an overview. J. Exp. Mar. Biol. Ecol. 1996, 200:57-66.
23. English T.E., Storey K.B. Freezing and anoxia stresses induce expression of metallothionein in the foot muscle and hepatopancreas of the marine gastropod Littorina littorea. J. Exp. Biol. 2003, 206:2517-2524.
24. 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, 15:111-127.
25. Forbes V.E., Depledge M.H. Environmental stress and the distribution of traits within populations. ECOtoxicology: Ecological Dimensions 1996, 71-86. Chapman & Hall, London. D.J. Baird, L. Maltby, P.W. Greig-Smith, P.E.T. Douben (Eds.).
26. Ghoshal K., Jacob S.T. Regulation of metallothionein gene expression. Prog. Nucleic Acid Res. Mol. Biol. 2000, 66:357-384.
27. Giacconi R., Bonfigli A.R., Testa R., Sirolla C., Cipriano C., Marra M., Malavolta M., Lattanzio F., Mocchegiani E. Implications of +647 A/C MT1A polymorphism in type 2 diabetes. Gerodontology 2009, 57:189-193.
28. Gillespie R.B., Guttman S.I. Effects of contaminants on the frequencies of allozymes in populations of the central stoneroller. Environ. Toxicol. Chem. 1989, 8:309-317.
29. Gillespie R.B., Guttman S.I. Correlations between water quality and frequencies of allozyme genotypes in spotfin shiner (Notropis spilopteris) populations. Environ. Pollut. 1993, 81:147-150.
30. Gillespie R.B., Guttman S.I. Chemical-induced changes in the genetic structure of populations: effects on allozymes. Genetics and Ecotoxicology 1999, 55-77. Taylor and Francis, Philadelphia. V.E. Forbes (Ed.).
31. Hamer D.H. Metallothionein1,2. Annu. Rev. Biochem. 1986, 55:913-951.
32. Hayashi Y., Hashizume T., Wakida K., Satoh M., Uchida Y., Watabe K., Matsuyama Z., Kimura A., Inuzuka T., Hozumi I. Association between metallothionein genes polymorphisms and sporadic amyotrophic lateral sclerosis in a Japanese population. Amyotroph. Lateral Scler 2006, 7:22-26.
33. Hill M.O., Smith A.J.E. Principal component analysis of taxonomic data with multi-state discrete characters. Taxon 1976, 25:249-255.
34. Hirose M., Sugimoto E., Sasaki R., Chiaa H. Crystallization and reaction mechanism of yeast phosphoglucomutase. J. Biochem. (Tokyo) 1970, 68:449-457.
35. Huvet A., Lapègue S., Magoulas A., Boudry P. Mitochondrial and nuclear DNA phylogeography of Crassostrea angulata, the Portuguese oyster endangered in Europe. Conserv. Genet. 2000, 1:251-262.
36. Isani G., Andreani G., Kindt M., Carpene E. Metallothioneins (MTs) in marine molluscs. Cell. Mol. Biol. 2000, 46:311-330.
37. Janssens T.K.S., Mariën J., Cenijn P., Legler J., Van Straalen N.M., Roelofs D. Recombinational micro-evolution of functionally different metallothionein promoter alleles from Orchesella cincta. BMC Evol. Biol. 2007, 7.
38. Janssens T.K.S., Lopéz R.D.R., Mariën J., Timmermans M.J.T.N., Montagne-Wajer K., Van Straalen N.M., Roelofs D. Comparative population analysis of metallothionein promoter alleles suggests stress-induced microevolution in the field. Environ. Sci. Technol. 2008, 42:3873-3878.
39. Janssens T.K.S., Roelofs D., Van Straalen N.M. Molecular mechanisms of heavy metal tolerance and evolution in invertebrates. Insect Sci. 2009, 16:3-18.
40. Johnson M.S., Black R. Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 1984, 38:1371-1383.
41. Kita K., Miura N., Yoshida M., Yamazaki K., Ohkubo T., Imai Y., Naganuma A. Potential effect on cellular response to cadmium of a single-nucleotide A→G polymorphism in the promoter of the human gene for metallothionein IIA. Hum. Genet. 2006, 120:553-560.
42. Klaassen C.D., Liu J., Choudhuri S. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu. Rev. Pharmacol. Toxicol. 1999, 39:267-294.
43. Kojima Y., Kagi J.H.R. Metallothionein. Trends Biochem. Sci 1978, 3:90-93.
44. Kraepiel A.M.L., Chiffoleau J.-F., Martin J.-M., Morel F.M.M. Geochemistry of trace metals in the Gironde estuary. Geochim. Cosmochim. Acta 1997, 61:1421-1436.
45. Lenfant P. Heterozygotie et valeur selective: le cas du poisson marin, Diplodus sargus (Linne, 1758). C.R. Biol. 2002, 325:239-252.
46. Lessios H.A. Testing electrophoretic data for agreement with Hardy-Weinberg expectations. Mar. Biol. 1992, 112:517-523.
47. Ma X.L., Cowles D.L., Carter R.L. Effect of pollution on genetic diversity in the bay mussel Mytilus galloprovincialis and the acorn barnacle Balanus glandula. Mar. Environ. Res. 2000, 50:559-563.
48. Maes G.E., Raeymaekers J.A.M., Pampoulie C., Seynaeve A., Goemans G., Belpaire C., Volckaert F.A.M. The catadromous European eel Anguilla anguilla (L.) as a model for freshwater evolutionary ecotoxicology: relationship between heavy metal bioaccumulation, condition and genetic variability. Aquat. Toxicol. 2005, 73:99-114.
49. Marchand J., Quiniou L., Riso R., Thebaut M.T., Laroche J. Physiological cost of tolerance to toxicants in the European flounder Platichthys flesus, along the French Atlantic Coast. Aquat. Toxicol. 2004, 70:327-343.
50. Maynard Smith J., Haigh J. The hitch-hiking effect of a favorable gene. Genet. Res. 1974, 23:23-35.
51. Meistertzheim, A.L., 2008. Capacité d'adaptation d'une espèce invasive, l'huître creuse du Pacifique Crassostrea gigas, en région Bretagne. Thèse de Doctorat de l'Université de Bretagne Occidentale. Western Brittany University, France, p. 188.
52. Menesguen, A., Aminot, A., Belin, C., Chapelle, A., Guillaud, J.-F., Joanny, M., Lefebvre, A., Merceron, M., Piriou, J.-Y. Souchu, P., 2001. L'eutrophisation des eaux marines et saumâtres en Europe, en particulier en France. IFREMER, 59 pp.
53. Miura N. Individual susceptibility to cadmium toxicity and metallothionein gene polymorphisms: with references to current status of occupational cadmium exposure. Ind. Health 2009, 47:487-494.
54. Moraga D., Tanguy A. Effects of anthropogenic factors on genetic diversity in the marine bivalve Crassostrea gigas: search for genetic markers. Vie Milieu 1997, 47:355-365.
55. Moraga D., Tanguy A. Genetic indicators of herbicide stress in the Pacific oyster Crassostrea gigas under experimental conditions. Environ. Toxicol. Chem. 2000, 19:706-711.
56. Murphy B.J., Andrews G.K., Bittel D., Discher D.J., McCue J., Green C.J., Yanovsky M., Giaccia A., Sutherland R.M., Laderoute K.R., Webster K.A. Activation of metallothionein gene expression by hypoxia involves metal response elements and metal transcription factor-1. Cancer Res. 1999, 59:1315-1322.
57. Nevo E., Lavie E., Ben-Shlomo R. Selection of allelic isozyme polymorphisms in marine organisms: pattern, theory, and application. Isozymes 1983, 10:69-92.
58. Nevo E., Ben-Shlomo R., Lavie B. Mercury selection of allozymes in marine organisms: prediction and verification in nature. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:1258-1259.
59. Nevo E., Noy R., Latvie B., Beiles A., Muchtar S. Genetic diversity and resistance to marine pollution: theory and practice. Biol. J. Linn. Soc. Lond. 1986, 29:139-144.
60. Nevo E. Evolution of genome-phenome diversity under environmental stress. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:6233-6240.
61. Nordberg M. Metallothioneins: historical review and state of knowledge. Talanta 1998, 46:243-253.
62. Ozols J. Degradation of hepatic stearyl CoA delta 9-desaturase. Mol. Biol. Cell 1997, 8:2281-2290.
63. Ray W.J., Roscelli G.A. A kinetic study of the phosphoglucomutase pathway. J. Biol. Chem. 1964, 239:1228-1236.
64. Raymond M., Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 1995, 86:248-249.
65. 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, 351:83-89.
66. 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, 122:1593-1596.
67. RNO, 2001. Surveillance du milieu marin. Travaux du Réseau National d'Observation de la qualité du milieu, Edition 2001. IFREMER et Ministère de l'Aménagement du Territoire et de l'Environnement, ISSN:1620-1124.
68. RNO, 2003. Surveillance du milieu marin. Travaux du Réseau National d'Observation de la qualité du milieu, Edition 2003. IFREMER et Ministère de l'Ecologie et du Développement Durable, ISSN:1620-1124.
69. RNO, 2006. Surveillance du Milieu Marin. Travaux du Réseau National d'Observation de la qualité du milieu, Edition 2006. IFREMER et Ministère de l'Ecologie et du Développement Durable, ISSN:1620-1124.
70. Roelofs D., Overhein L., de Boer M.E., Janssens T.K.S., van Straalen N.M. Additive genetic variation of transcriptional regulation: metallothionein expression in the soil insect Orchesella cincta. Heredity 2005, 96:85-92.
71. Roesijadi G. Metallothionein and its role in toxic metal regulation. Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol. 1996, 113:117-123.
72. SAGE Vilaine Projet de schéma d'aménagement et de gestion des eaux de la Vilaine, Atlas 2000, Institut d'Aménagement de la Vilaine, La Roche Bernard, France.
73. Stanton M.L., Roy B.A., Thiede D.A. Evolution in stressful environments. I. Phenotypic variability, phenotypic selection, and response to selection in five distinct environmental stresses. Evolution 2000, 54:93-111.
74. Strohman R.C., Moss P.S., Micou-Eastwood J., Spector D., Przybyle A., Patterson B. Messenger RNA for myosin polypeptides: isolation from single myogenic cell cultures. Cell 1977, 10:265-273.
75. Tanguy A., Fernandez Castro N., Marhic A., Moraga D. Effects of an organic pollutant (tributyltin) on genetic structure in the pacific oyster Crassostrea gigas. Mar. Pollut. Bull. 1999, 38:550-559.
76. Tanguy A., Moraga D. Cloning and characterization of a gene coding for a novel metallothionein in the Pacific oyster Crassostrea gigas (CgMT2): a case of adaptive response to metal-induced stress?. Gene 2001, 273:123-130.
77. Tanguy A., Mura C., Moraga D. Cloning of a metallothionein gene and characterization of two other cDNA sequences in the Pacific oyster Crassostrea gigas (CgMT1). Aquat. Toxicol. 2001, 55:35-47.
78. Tanguy A., Boutet I., Bonhomme F., Boudry P., Moraga D. Polymorphism of metallothionein genes in the Pacific oyster Crassostrea gigas as a biomarker of response to metal exposure. Biomarkers 2002, 7:439-450.
79. 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.
80. Tanguy A., Boutet I., Laroche J., Moraga D. Molecular identification and expression study of differentially regulated genes in the Pacific oyster Crassostrea gigas in response to pesticide exposure. FEBS J. 2005, 272:390-403.
81. Tanguy A., Boutet I., Moraga D. Molecular characterization of the glutamine synthetase gene in the Pacific oyster Crassostrea gigas: expression study in response to xenobiotic exposure and developmental stage. Biochim. Biophys. Acta: Gene. Struct. Expr. 2005, 1681:116-125.
82. Tanguy A., Boutet I., Boudry P., Degremont L., Laroche J., Moraga D. Molecular identification and expression of the phosphoglucomutase (PGM) gene from the Pacific oyster Crassostrea gigas. Gene 2006, 382:20-27.
83. Tate S.S., Leu F.Y., Meister A. Rat liver glutamine synthetase. Preparation, properties, and mechanism of inhibition by carbamyl phosphate. J. Biol. Chem. 1972, 247:5312-5321.
84. Theodorakis C.W. Integration of genotoxic and population genetic endpoints in biomonitoring and risk assessment. Ecotoxicology 2001, 10:245-256.
85. Theodorakis C.W., Wirgin I.I. Genetic responses as population-level biomarkers of stress in aquatic ecosystems. Biological Indicators of Aquatic Ecosystem Stress 2002, 149-186. American Fisheries Society, Bethesda, Maryland. S.M. Adams (Ed.).
86. Timmermans M.J.T.N., Ellers J., Van Straalen N.M. Allelic diversity of metallothionein in Orchesella cincta (L.): Traces of natural selection by environmental pollution. Heredity 2007, 98:311-319.
87. Valavanidis A., Vlahogianni T., Dassenakis M., Scoullos M. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol. Environ. Safe. 2006, 64:178-189.
88. Van Straalen N.M. Genetic biodiversity in toxicant-stressed populations. Prog. Environ. Sci. 1999, 1:195-201.
89. Van Straalen N.M., Timmermans M.J.T.N. Genetic variation in toxicant-stressed populations: an evaluation of the genetic erosion hypothesis. Hum. Ecol. Risk Assess. 2002, 8:983-1002.
90. Varshney U., Hoar D.I., Starozik D., Gedamu L. A frequent restriction fragment length polymorphism in the human metallothionein-II processed gene region is evolutionarily conserved. Mol. Biol. Med. 1984, 2:193-206.
91. Viarengo A., Nott J.A. Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol. 1993, 104:355-372.
92. Waeles M., Riso R.D., Le Corre P. Seasonal variations of dissolved and particulate copper species in estuarine waters. Estuar. Coast. Shelf Sci. 2005, 62:313-323.
93. Waeles M., Riso R.D., Le Corre P. Distribution and seasonal changes of lead in an estuarine system affected by agricultural practices: the Penzé estuary, NW France. Estuar. Coast. Shelf Sci. 2007, 74:570-578.
94. Watanabe T., Shimizu A., Ohno K., Masaki S., Kondo K. Restriction fragment length variations and chromosome mapping of two mouse metallothionein genes, Mt-1 and Mt-2. Biochem. Genet. 1989, 27:689-697.
95. Wirgin I.I., Theodorakis C.W. Molecular biomarkers in aquatic organisms: DNA damage and RNA expression. Biological Indicators of Aquatic Ecosystem Stress 2002, 43-110. American Fisheries Society Bethesda, Maryland. S.M. Adams (Ed.).
96. Yap C.K., Tan S.G., Ismail A., Omar H. Allozyme polymorphisms and heavy metal levels in the green-lipped mussel Perna viridis (Linnaeus) collected from contaminated and uncontaminated sites in Malaysia. Environ. Int. 2004, 30:39-46.