Interactive effects of cadmium and hypoxia on metabolic responses and bacterial loads of eastern oysters Crassostrea virginica Gmelin

Chemosphere

Volumn 82, Issue 3, 2011, Pages 377-389

  Ivanina, Anna V ^a   Froelich, Brett ^a   Williams, Tiffany ^a   Sokolov, Eugene P ^b   Oliver, James D ^a   Sokolova, Inna M ^a  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^b CAROLINAS MEDICAL CENTER   (United States)

Author keywords

Aerobic metabolism; Bivalves; Energy status; Glycolysis; Transcript expression; Vibrio spp.

Indexed keywords

CADMIUM; ENZYMES; ESTUARIES; MARINE POLLUTION; METABOLISM; SHELLFISH; TISSUE;

BIVALVES; ENERGY STATUS; GLYCOLYSIS; TRANSCRIPT EXPRESSION; VIBRIO SPP;

MOLLUSCS;

CADMIUM; CITRATE SYNTHASE; CYTOCHROME C OXIDASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCOSE; GLYCOGEN; HEXOKINASE; MESSENGER RNA;

ACCLIMATION; BACTERIUM; BENTHOS; BIOACCUMULATION; BIVALVE; CADMIUM; CATABOLISM; COASTAL ZONE; ENZYME ACTIVITY; ESTUARINE ENVIRONMENT; FOOD CHAIN; GLUCOSE; HOMEOSTASIS; HYPOXIA; MITOCHONDRION; PHYSIOLOGICAL RESPONSE; TOXIC MATERIAL;

ACCLIMATIZATION; AEROBIC METABOLISM; ANAEROBIC METABOLISM; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL FLORA; BIOACCUMULATION; CARBOHYDRATE METABOLISM; CATABOLISM; CONTROLLED STUDY; ENZYME ACTIVITY; ESTUARY; GENE EXPRESSION; HYPOXIA; METABOLIC RATE; METABOLIC REGULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGEN CONSUMPTION; OYSTER; SEA POLLUTION; SURVIVAL; TISSUE LEVEL; VIBRIO PARAHAEMOLYTICUS; VIBRIO VULNIFICUS;

BACTERIA (MICROORGANISMS); BIVALVIA; CRASSOSTREA VIRGINICA; OSTREIDAE; VIBRIO; VIBRIO PARAHAEMOLYTICUS; VIBRIO VULNIFICUS;

EID: 78650073949     PISSN: 00456535     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2010.09.075     Document Type: Article

References (86)

1. Baghdiguian S., Riva A. Metabolic modifications brought by the synergic action of cadmium and experimental starvation of clams Ruditapes decussatus. Mar. Environ. Res. 1985, 17:289.
2. Baker S.M., Mann R. Effects of hypoxia and anoxia on larval settlement, juvenile growth, and juvenile survival of the oyster Crassostrea virginica. Biol. Bull. 1992, 182:265-296.
3. Belaidi E., Beguin P.C., Levy P., Ribuot C., Godin G.-R. Prevention of HIF-1 activation and iNOS gene targeting by low-dose cadmium results in loss of myocardial hypoxic preconditioning in the rat. Am. J. Physiol. - Heart Circ. Physiol. 2008, 294:H901-H908.
4. Bell, H.J., Inoue, T., Syed, N.I., 2008. A Peripheral Oxygen Sensor Provides Direct Activation of an Identified Respiratory CPG Neuron in Lymnaea, pp. 25-29.
5. Bergmeyer, H.U., 1985. Methods of enzymatic analysis. Vol VI. Metabolites 1: Carbohydrates. Vol. VIII. Metabolites 3: Lipids, Amino Acids and Related Compounds VCH Verlagsgesellschaft, Weinheim.
6. Bhattacharya, M., Choudhury, P., Kumar, R., 2000. Antibiotic- and metal-resistant strains of Vibrio parahaemolyticus isolated from shrimps. Microbial Drug Resistance 6, 171-172. doi:. doi:10.1089/107662900419492.
7. Birch Machin M.A., Turnbull D.M. Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods in Cell Biology 2001, vol. 65:97-117. Academic Press, San Diego etc.
8. Brahimi-Horn M.C., Pouyssegur J. Oxygen, a source of life and stress. FEBS Lett. 2007, 581:3582-3591.
9. Calow P. Proximate and ultimate responses to stress in biological systems. Biol. J. Linnean Soc. 1989, 37:173-181.
10. Calow P. Physiological costs of combating chemical toxicants: Ecological implications. Comp. Biochem. Physiol. Part C: Comp. Pharmacol. 1991, 100:3-6.
11. Cherkasov A.S., Ringwood A.H., Sokolova I.M. Effects of cadmium exposure on mitochondrial function are modulated by acclimation temperature in eastern oysters Crassostrea virginica Gmelin (Bivalvia: Ostreidae). Environ. Toxicol. Chem. 2006, 25:2461-2469.
12. Cherkasov A.S., Biswas P.K., Ridings D.M., Ringwood A.H., Sokolova I.M. Effects of acclimation temperature and cadmium exposure on cellular energy budgets in a marine mollusk Crassostrea virginica: linking cellular and mitochondrial responses. J. Exp. Biol. 2006, 209:1274-1284.
13. Cherkasov A.A., Overton R.A., Sokolov E.P., Sokolova I.M. Temperature dependent effects of cadmium and purine nucleotides on mitochondrial aconitase from a marine ectotherm, Crassostrea virginica: a role of temperature in oxidative stress and allosteric enzyme regulation. J. Exp. Biol. 2007, 210:46-55.
14. Cherkasov A.S., Taylor C., Sokolova I.M. Seasonal variation in mitochondrial responses to cadmium and temperature in eastern oysters Crassostrea virginica (Gmelin) from different latitudes. Aquat. Toxicol. 2010, 97:68-78.
15. Chun Y.S., Choi E., Kim G.T., Choi H., Kim C.H., Lee M.J., Kim M.S., Park J.W. Cadmium blocks hypoxia-inducible factor (HIF)-1-mediated response to hypoxia by stimulating the proteasome-dependent degradation of HIF-1a. Eur. J. Biochem. 2000, 267:4198-4204.
16. Colwell R.R. A global and historical perspective of the genus Vibrio. The Biology of Vibrios 2006, 3-11. American Society for Microbiology, Washington, DC. F.L. Thompson (Ed.).
17. Crompton, T.R., 1997. Toxicants in Aqueous Ecosystem. John Wiley and Sons, Chichester, New York, Weinheim, Brisbane, Singapore, Toronto.
18. 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.
19. Diaz R.J., Rosenberg R. Spreading dead zones and consequences for marine ecosystems. Science 2008, 321:926-929. 10.1126/science.1156401.
20. Diaz R.J., Solow A. Ecological and economic consequences of hypoxia, topic 2: report for the integrated assessment on hypoxia in the Gulf of Mexico. NOAA Coast. Ocean Prog. Decis. Anal. Ser. 1999, 16:1-63.
21. El-Hendawy H.H., Ali D.A., Enas H., El-Shatoury H., Ghanem S.M. Bioaccumulation of heavy metals by Vibrio alginolyticus isolated from wastes of iron and steel factory, Helwan, Egypt. Egypt. Acad. J. Biol. Sci. 2009, 1:23-28.
22. Fridlyand L.E., Ma L., Philipson L.H. Adenine nucleotide regulation in pancreatic {beta}-cells: modeling of ATP/ADP-Ca2+ interactions. Am. J. Physiol. - Endocrinol. Metab. 2005, 289:E839-848. 10.1152/ajpendo.00595.2004.
23. Fulladosa E., Murat J., Villaescusa I. Effect of Cadmium(II), Chromium(VI), and Arsenic(V) on Long-Term Viability- and Growth-Inhibition Assays Using Vibrio fischeri Marine Bacteria. Arch. Environ. Contam. Toxicol. 2005, 49:299-306.
24. Gauthier M., Flatau G. Concentration and method of cadmium fixation by a marine Vibrio. CR Acad. Sci. Hebd. Seances Acad. Sci. D 1977, 285:817-820.
25. GESAMP, 1987. Land-sea boundary flux of contaminants: contributions from rivers. Group of Experts on the Scientific Aspects of Marine Environmental Protection (GESAMP) Reports and Studies 32, 1-172.
26. Greenway S.G., Storey K.B. The effect of prolonged anoxia on enzyme activities in oysters (Crassostrea virginica) at different seasons. J. Exp. Mar. Biol. Ecol. 1999, 242:259-272.
27. Grieshaber M., Kronig E., Koormann R. A photometric estimation of phospho-l-arginine, arginine and octopine using homogeneous octopine dehydrogenase isozyme 2 from the squid, Loligo vulgaris Lam. Hoppe-Seylers Zeitschrift Fur Physiologische Chemie 1978, 359:133-136.
28. Hackney, C.T., Grimley, J., Posey, M., Alphin, T., Hyland, J., 1998. Sediment Contamination in North Carolina's Estuaries. Publication # 198 of the Center For Marine Science Research, University of North Carolina at Wilmington, pp. 2-59.
29. Hattink J., Boeck G.D., Blust R. The toxicokinetics of cadmium in carp under normoxic and hypoxic conditions. Aquat. Toxicol. 2005, 75:1.
30. Hattink J., De Boeck G., Blust R. Toxicity, accumulation, and retention of zinc by carp under normoxic and hypoxic conditions. Environ. Toxicol. Chem. 2006, 25:89-96.
31. Heijnen J.J., van Gulik W.M., Shimizu H., Stephanopoulos G. Metabolic flux control analysis of branch points: an improved approach to obtain flux control coefficients from large perturbation data. Metab. Eng. 2004, 6:391-400.
32. Hoogewijs D., Terwilliger N.B., Webster K.A., Powell-Coffman J.A., Tokishita S., Yamagata H., Hankein T., Burmester T., Rytokonen K.T., Nikinmaa M., Abele D., Heise K., Lucassen M., Fandrey J., Maxwell P.H., Pahlman S., Gorr T.A. From critters to cancers: bridging comparative and clinical research on oxygen sensing, HIF signaling, and adaptations towards hypoxia. Integr. Comp. Biol. 2007, 1:26.
33. Horiguchi H., Kayama F., Oguma E., Willmore W.G., Hradecky P., Bunn H.F. Cadmium and platinum suppression of erythropoietin production in cell culture: clinical implications. Blood 2000, 96:3743-3747.
34. Hu C.-J., Wang L.-Y., Chodosh L.A., Keith B., Simon M.C. Differential roles of hypoxia-inducible factor 1a(HIF-1a) and HIF-2a in hypoxic gene regulation. Mol. Cell. Biol. 2003, 23:9361-9374.
35. Jeneson J.A.L., Westerhoff H.V., Kushmerick M.J. A metabolic control analysis of kinetic controls in ATP free energy metabolism in contracting skeletal muscle. Am. J. Physiol. - Cell Physiol. 2000, 279:C813-832.
36. Kazmi S.U., Roberson B.S., Stern N.J. Cadmium chloride susceptibility, a characteristic of Campylobacter spp. J. Clin. Microbiol. 1985, 21:708-710.
37. Keppler D., Decker K. Glycogen. Methods of Enzymatic Analysis 1984, 11-18. Verlag Chemie, Weinheim etc. H.U. Bergmeyer (Ed.).
38. Koga T., Takumi K. Comparision of cross-protection against some enviromental stresses between cadmium-adapted and heat-adapted cells of Vibrio Parahaemolyticus. J. Gen. Appl. Microbiol. 1995, 41.
39. Kurochkin I.O., Ivanina A.V., Eilers S., Downs C.A., May L.A., Sokolova I.M. Cadmium affects metabolic responses to prolonged anoxia and reoxygenation in eastern oysters Crassostrea virginica. AJP - Regul. Integr. Comp. Physiol. 2009, 00324:2009.
40. Lannig G., Cherkasov A.S., Sokolova I.M. Temperature-dependent effects of cadmium on mitochondrial and whole-organism bioenergetics of oysters (Crassostrea virginica). Mar. Environ. Res. 2006, 62:S79-S82.
41. Lannig G., Flores J.F., Sokolova I.M. Temperature-dependent stress response in oysters, Crassostrea virginica: pollution reduces temperature tolerance in oysters. Aquat. Toxicol. 2006, 79:278-287.
42. Lannig G., Bock C., Cherkasov A., Pörtner H.O., Sokolova I.M. Cadmium-dependent oxygen limitation affects temperature tolerance in eastern oysters (Crassostrea virginica Gmelin). Am. J. Physiol. - Regul., Integr. Comp. Physiol. 2008, 294:1338-1346.
43. Larade K., Storey K.B. A profile of metabolic responses to anoxia in marine invertebrates. Sensing Signaling and Cell Adaptation 2002, 27-46. Elsevier Science B.V. K.B. Storey, J.M. Storey (Eds.).
44. Larade K., Storey K.B. Living without oxygen: anoxia-responsive gene expression and regulation. Curr. Genomics 2009, 10:76-85.
45. Le Moullac G., Queau I., Le Souchu P., Pouvreau S., Moal J., Le Coz J.R., Damain J.F. Metabolic adjustments in the oyster Crassostrea gigas according to oxygen level and temperature. Mar. Biol. Res. 2007, 3:357-366.
46. Legeay A., Achard-Joris M., Baudrimont M., Massabuau J.C., Bourdineaud J.P. Impact of cadmium contamination and oxygenation levels on biochemical responses in the Asiatic clam Corbicula fluminea. Aquat. Toxicol. 2005, 74:242-253. 10.1016/j.aquatox.2005.05.015.
47. Lenihan H.S., Peterson C.H., Byers J.E., Grabowski J.H., Thayer G.W., Colby D.R. Cascading of habitat degradation: oyster reefs invaded by refugee fishes escaping stress. Ecol. Appl. 2001, 11:764-782.
48. +-ATPase in eel, Anguilla anguilla, intestine and gills. Comp. Biochem. Physiol. - Part A: Mol. Integr. Physiol. 1998, 120:89-91.
49. Lionetto M.G., Giordano M.E., Vilella S., Schettino T. Inhibition of eel enzymatic activities by cadmium. Aquat. Toxicol. 2000, 48:561-571.
50. Lucassen M., Schmidt A., Eckerle L.G., Pörtner H.-O. Mitochondrial proliferation in the permanent vs. temporary cold: enzyme activities and mRNA levels in Antarctic and temperate zoarcid fish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 285:R1410-1420. 10.1152/ajpregu.00111.2003.
51. Morley S.A., Lurman G.J., Skepper J.N., Pörtner H.O., Peck L.S. Thermal plasticity of mitochondria: a latitudinal comparison between southern ocean molluscs. Comp. Biochem. Physiol., Part A 2009, 152:423-430.
52. Moyes C.D., LeMoine C.M.R. Control of muscle bioenergetic gene expression: implications for allometric scaling relationship of glycolytic and oxidative enzymes. J. Exp. Biol. 2005, 208:1601-1610.
53. Nies D.H. Resistance to cadmium, cobalt, zinc, and nickel in microbes. Plasmid 1992, 27:17-28.
54. Obara N., Imagawa S., Nakano Y., Suzuki N., Yamamoto M., Nagasawa T. Suppression of erythropoietin gene expression by cadmium depends on inhibition of HIF-1, not stimulation of GATA-2. Arch. Toxicol. 2003, 77:267.
55. O'Connor T.P., Lauenstein G.G. Trends in chemical concentrations in mussels and oysters collected along the US coast: update to 2003. Mar. Environ. Res. 2006, 62:261-285.
56. Oliver J.D. Wound infections caused by Vibrio vulnificus and other marine bacteria. Epidemiol. Infect. 2005, 133:383-391.
57. Oliver J.D. Vibrio vulnificus. The Biology of Vibrios 2006, 349-366. American Society for Microbiology, Washington, DC. F.L. Thompson (Ed.).
58. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:2002-2007.
59. Pierron F., Baudrimont M., Boudou A., Massabuau J.C. Effects of salinity and hypoxia on cadmium bioaccumulation in the shrimp Palaemon longirostris. Environ. Toxicol. Chem. 2007, 26:1010-1017.
60. Pierron F., Baudrimont M., Gonzalez P., Bourdineaud J.P., Elie P. Common pattern of gene expression in response to hypoxia or cadmium in the gills of the European glass eel (Anguilla anguilla). Environ. Sci. Technol. 2007, 41:3005-3011.
61. Pigeot J., Miramand P., Guyot T., Sauriau P.G., Fichet D., Le Moine O., Huet V. Cadmium pathways in an exploited intertidal ecosystem with chronic cadmium inputs (Marennes-Oleron, Atlantic coast, France). Mar. Ecol. Prog. Ser. 2006, 307:101-114.
62. Rabalais N.N., Turner R.E., Justič D., Dortch Q., Wiseman W.J.J. Characterization of hypoxia, Topic 1: Report for the integrated assessment on hypoxia in the Gulf of Mexico. NOAA Coast. Ocean Prog. Decis. Anal. Ser. 1999, 15:1-203.
63. Roesijadi, G., 1996. Environmental factors: response to metals. In: Kennedy, V.S., Newell, R.I.E., Eble, A.F. (Eds.), The Eastern Oyster Crassostrea virginica. A Maryland Sea Grant Book, College Park Maryland, pp. 515-537.
64. Sanni B., Williams K., Sokolov E.P., Sokolova I.M. Effects of acclimation temperature and cadmium exposure on mitochondrial aconitase and LON protease from a model marine ectotherm, Crassostrea virginica. Comp. Biochem. Physiol., Part C 2008, 147:101-112.
65. Semenza G.L. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 2004, 19:176-182.
66. Semenza G.L. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem. J. 2007, 405:1-9.
67. Sibly R.M., Calow P. A life-cycle theory of responses to stress. Biol. J. Linn. Soc. 2009, 37:101-116.
68. Sidell B.D., Driedzic W.R., Stowe D.B., Johnston I.A. Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol. Zool. 1987, 60:221-232.
69. Siu P.M., Donley D.A., Bryner R.W., Alway S.E. Citrate synthase expression and enzyme activity after endurance training in cardiac and skeletal muscle. J. Appl. Physiol. 2003, 94:555-560.
70. Sokolova I.M. Cadmium effects on mitochondrial function are enhanced by elevated temperatures in a marine poikilotherm, Crassostrea virginica Gmelin (Bivalvia: Ostreidae). J. Exp. Biol. 2004, 207:2639-2648.
71. Sokolova I.M., Lannig G. Interactive effects of metal pollution and temperature on metabolism in aquatic ectotherms: implications of global climate change. Climate Res. 2008, 37:181-201.
72. Sokolova I.M., Bock C., Pörtner H.O. Resistance to freshwater exposure in White Sea Littorina spp. I. Anaerobic metabolism and energetics. J. Comp. Physiol. B. 2000, 170:91-103.
73. Sokolova I.M., Ringwood A.H., Johnson C. Tissue-specific accumulation of cadmium in subcellular compartments of eastern oysters Crassostrea virginica Gmelin (Bivalvia: Ostreidae). Aquat. Toxicol. 2005, 74:218-228.
74. Soñanez-Organis J.G., Peregrino-Uriarte A.B., Gómez-Jiménez S., López-Zavala A., Forman H.J., Yepiz-Plascencia G. Molecular characterization of hypoxia inducible factor-1 (HIF-1) from the white shrimp Litopenaeus vannamei and tissue-specific expression under hypoxia. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2009, 150:395-405.
75. Stohs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 1995, 18:321-336.
76. Storey K.B., Storey J.M. Metabolic rate depression in animals: transcriptional and translational controls. Biol. Rev. 2004, 79:207-233. doi:10.1017/S1464793103006195.
77. Strydom C., Robinson C., Pretorius E., Whitcutt J.M., Marx J., Bornman M.S. The effect of selected metals on the central metabolic pathways in biology: a review. Water Air Soil Pollut. 2006, 32:543-554.
78. Suzuki S., Fukagawa T., Takama K. Occurrence of tributyltin-tolerant bacteria in tributyltin- or cadmium-containing seawater. Appl. Environ. Microbiol. 1992, 58:3410-3412.
79. Taylor C.T. Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem. J. 2008, 409:19-26.
80. Thompson F.L., Swings J. Taxonomy of the Vibrios. The Biology of Vibrios 2006, 29-43. American Society for Microbiology, Washington, DC. F.L. Thompson (Ed.).
81. Toth D., Ferianc P., Karelova E., Polek B. Protein expression in the stressed Vibrio strains. Ann. N. Y. Acad. Sci. 1996, 782:252-263.
82. Vaquer-Sunyer R., Duarte C.M. Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences 2008, 105:15452-15457. 10.1073/pnas.0803833105.
83. Webster K.A. Evolution of the coordinate regulation of glycolytic enzyme genes by hypoxia. J. Exp. Biol. 2003, 206:2911-2922.
84. Webster K.A. Hypoxia: life on the edge. Antioxid. Redox Signaling 2007, 9:1303-1308. doi:10.1089/ars.2007.1730.
85. Xing D., Bonanno J.A. Hypoxia preconditioning protection of corneal stromal cells requires HIF1α but not VEGF. Mol. Vision 2009, 15:1020-1027.
86. Ziello J.E., Jovin I.S., Huang Y. Hypoxia-inducible factor(HIF)-1 regulatory pathway and its potential for therapeutic intervention in malignancy and ischemia. Yale J. Biol. Med. 2007, 80:51-60.