Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-12T15:09:13.220Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of sediment nearness on the metabolic enzyme activityand energy state of the oyster Crassostrea gigas

Published online by Cambridge University Press:  27 October 2007

Gilles Le Moullac ,
Pierre-Gildas Fleury ,
Jean-René Le Coz ,
Jeanne Moal  and
Jean-François Samain
Gilles Le Moullac
Affiliation:
IFREMER, UMR 100 Physiologie et Ecophysiologie des Mollusques marins, Site Expérimental d'Argenton, 29840 Argenton en Landunvez, France
Pierre-Gildas Fleury
Affiliation:
IFREMER, Laboratoire Environnement-Ressources, 12 rue des Résistants, BP 26, 56470 La Trinité sur Mer, France
Jean-René Le Coz
Affiliation:
IFREMER, UMR 100 Physiologie et Ecophysiologie des Mollusques marins, Centre de Brest, BP 70, 29280 Plouzané, France
Jeanne Moal
Affiliation:
IFREMER, UMR 100 Physiologie et Ecophysiologie des Mollusques marins, Centre de Brest, BP 70, 29280 Plouzané, France
Jean-François Samain
Affiliation:
IFREMER, UMR 100 Physiologie et Ecophysiologie des Mollusques marins, Centre de Brest, BP 70, 29280 Plouzané, France
Get access

Abstract

This study was designed to assess in situ the effects of sediment nearness on Crassostrea gigas metabolism. One year-old oysters were reared for 5 months (April-August) in plastic bags on metallic frames at 10 and 60 cm off the sediment at the beginning of April. The management of the energetic resources (storage, consumption) was estimated with respect to biochemical changes of proteins, lipids and carbohydrates. In order to evaluate the effect of the sediment nearness at cellular level, the metabolic rate was evaluated by assessing pyruvate kinase (PK) and phosphoenolpyruvate carboxykinase (PEPCK) enzyme activities and electron transport system (ETS) activity. The metabolic pathways were assessed by measuring ATP and intermediary metabolites such as alanine, succinate and aspartate. Despite similar survival and growth at the two rearing levels, the protein, lipid and carbohydrate content were significantly lower in the oysters close to the bottom. In the oysters reared at 10 cm, PK activity was also significantly reduced and a significant negative correlation between alanine content and PK activity was revealed. The sediment nearness decreased significantly the ATP content in the oyster. There was a significant relationship between ATP and aspartate in these oysters. The use of aspartate contributed to complete the metabolic pathways along with carbohydrate allowing to maintain the same biological performance as the oyster reared far from the bottom. The energy state (proteins, lipids, carbohydrates and ATP contents) could suggest that the oysters close to the sediment were fed less but the metabolic enzyme activities allow to suggest an oxygen deficiency. However, the reduced PK activity, the absence of PEPCK activity stimulation and the utilization of aspartate suggest a transition stage to anaerobiosis.

Keywords

OysterSedimentMetabolismProteinsLipidsCarbohydrateAlanineSuccinateAspartate
Type
Research Article
Information
Aquatic Living Resources , Volume 20 , Issue 3 , July 2007 , pp. 279 - 286
Copyright
© EDP Sciences, IFREMER, IRD, 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Berthelin, C., Kellner, K., Mathieu, M., 2000, Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (west coast of France). Comp. Biochem. Physiol. 125, 359-369. CrossRef
Bligh, E.G., Dyer, W.J., 1959, A rapid method for total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917. CrossRef
David, E., Tanguy, A., Pichavant, K., Moraga, D., 2005, Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS J. 272, 5635-5652. CrossRef
de Zwann A., 1983, Carbohydrate catabolism in bivalves. In: Hochacka P.W. (Ed.) The Mollusca (vol. 1) Metabolic biochemistry and molecular biomechanics. Academic Press, NY, pp. 137-175.
de Zwann, A., Cortesi, P., van den Thillart, G., Roos, J., Storey, K.B., 1991, Differential sensitivities to hypoxia by two anoxia tolerant marine molluscs: a biochemical analysis. Mar. Biol. 111, 343-351. CrossRef
de Zwann A., Mathieu M., 1992, Cellular Biochemistry and endocrinology. In: Gosling E. (Ed.) The mussel mytilus: ecology, physiology, genetics and culture. Elsevier, Amsterdam, pp. 223-293.
Delaporte, M., Soudant, P., Lambert, C., Moal, J., Pouvreau, S., Samain, J.F., 2006, Impact of food availability on energetic storage and defense related hemocyte parameters of the Pacific oyster Crassostrea gigas during an experimental reproductive cycle. Aquaculture 254, 571-582 CrossRef
Deslous-Paoli J.M., 1980. Contribution à l'étude de la biologie de l'huître C.gigas Thunberg dans le bassin et les claires de Marennes-Oléron. Thèse de 3ème cycle, Université d'Aix-Marseille II.
Diaz, R.J., Rosenberg, R., 1995, Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Ocean. Mar. Biol.: Annual Review 33, 245-303.
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., 1956, Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350-356. CrossRef
Dunphy, B.J., Wells, R.M.G., Jeffs, A.G., 2006, Oxygen consumption and enzyme activity of the subtidal flat oyster (Ostrea chilensis) and Pacific oyster (Crassostrea gigas): responses to temperature and starvation. NZ J. Mar. Freshwater Res. 40, 149-158. CrossRef
Encomio V.G., 1998, Respiratory and metabolic response to sulfide and hypoxia in the marine echiuran worm, Urechis caupo. San Francisco University, PhD Thesis.
Fanslow, D.L., Nalepa, T.F., Johengen, T.H., 2001, Seasonal changes in the respiratory electron transport system (ETS) and respiration of the zebra mussel, Dreissena polymorpha in Saginaw Bay, lake Huron.. Hydrobiologia 448, 61-70. CrossRef
Gagnaire B., Soletchnik P., Madec P., Geairon P., Le Moine O., Renault T., 2006, Diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg), reared at two heights above sediment in Marennes-Oléron Basin, France; Difference in mortality, sexual maturation and hemocyte parameters. Aquaculture 254, 606-616.
Garcia-Esquivel, Z., Bricelj, V.M., Gonzalez-Gomez, M.A., 2001, Physiological basis for energy demands and early postlarval mortality in the Pacific oyster, Crassostrea gigas. J. Exp. Mar. Biol. Ecol. 263, 77-103. CrossRef
Garcia-Esquivel, Z., Bricelj, V.M., Felbeck, H., 2002, Metabolic depression and whole-body response to enforced starvation by Crassostrea gigas postlarvae. Comp. Biochem. Physiol. 133A, 63–77 CrossRef
Goulletquer P., Soletchnik P., Le Moine O., Razet D., Geairon P., Faury N., Taillade S., 1998, Summer mortality of the Pacific cupped oyster Crassostrea gigas in the Bay of Marennes-Oléron (France). Cons. int. Explor. Mer, CM 1998 / CC 14.
Greenway, S.C., Storey, K.B., 1999, The effect of prolonged anoxia on enzyme activities in oysters (Crassostrea virginica) at different seasons. J. Exp. Mar. Biol. Ecol. 242, 259-272. CrossRef
Greenway, S.C., Storey, K.B., 2000, Seasonal change and prolonged anoxia affect the kinetic properties of phosphofructokinase and pyruvate kinase in oysters. J. Comp. Physiol. B 170, 285-293. CrossRef
Greenway, S.C., Storey, K.B., 2001, Effects of seasonal change and prolonged anoxia on metabolic enzymes of Littorina littorea. Can. J. Zool. 79, 907-915. CrossRef
Hicks, D.W., McMahon, R.F., 2002, Respiratory responses to temperature and hypoxia in the nonindigenous brown mussel, Perna perna (Bivalvia: Mytilidae), from the Gulf of Mexico. J. Exp. Mar. Biol. Ecol. 277, 61-78. CrossRef
Laudien, J., Schieck, D., Brey, T., Portner, H.O., Arntz, W.E., 2002, Survivorship of juvenile clams Donax serra (Bivalvia, Donacidae) exposed to severe hypoxia and hydrogen sulphide. J. Exp. Mar. Biol. Ecol. 271, 9-23. CrossRef
Le Moullac, G., Bacca, H., Huvet, A., Moal, J., Pouvreau, S., Van Wormhoudt, A., 2007, Transcriptional regulation of pyruvate kinase and phosphoenolpyruvate carboxykinase in the adductor muscle of the oyster Crassostrea gigas during prolonged hypoxia. J. Exp. Zool. 307A, 371-382. CrossRef
Le Moullac G., Quéau I., Le Souchu P., Pouvreau S., Moal J., Le Coz J.R., Samain J.F., 2007, Metabolic adjustments in the oyster Crassostrea gigas according to oxygen level and temperature. Mar. Biol. Res. in press.
Lesser, M.P., Kruse, V.A., 2004, Seasonal temperature compensation in the horse mussel, Modiolus modiolus: metabolic enzymes, oxidative stress and heat shock proteins. Comp. Biochem. Physiol. 137A, 495-504. CrossRef
Lowry, O.H., Rosenbrough, N., Farr, A.L., Randall, R.J., 1951, Protein measurement with Folin phenol reagent. J. Biol. Chem. 193, 265-275.
Madon, S.P., Schneider, D., Stoeckel, J.A., 1998, In situ estimation of zebra mussel metabolic rates using the electron transport system (ETS) assay. J. Shellfish Res. 17, 195-203.
Moal J., Le Coz J.R., Samain J.F., Daniel J.Y., 1989, Nucleotides in bivalves: extraction and analysis by high -performance liquid chromatography (HPLC). Comp. Biochem. Physiol., 93B, 307-316.
Mollering H., 1985, L-Aspartate and L-asparagine. In: Bergmeyer H.U. (Ed.) Methods in Enzymatic Analysis. 8 N° 3. Verlag Chemie, Weinheim, pp. 350-357.
Mori, K., Tamate, H., Imai, T., Itikawa, O., 1965, Changes in the metabolism of lipids and glycogen of the oyster during the stages of sexual maturation and spawning. Bull. Tohoku Reg. Fish. Res. Lab. 25, 65-88.
Mori, K., 1979, Effects of artificial eutrophication on the metabolism of the Japanese oyster Crassostrea gigas. Mar. Biol. 53, 361-369. CrossRef
Owens, T.G., King, F.D., 1975, The measurement of respiratory electron transport system activity in marine zooplankton. Mar. Biol. 30, 27-36. CrossRef
Perdue, J.A., Beattie, J.H., Chew, K.K., 1981, Some relationships between gametogenic cycle and summer mortality phenomenon in the pacific oyster (Crassostrea gigas) in Washington State. J. Shellfish Res. 1, 9-16.
Plaxton, W.C., Storey, K.B., 1984, Purification and properties of aerobic and anoxic forms of pyruvate kinase from red muscle organ of the channeled whelk, Busycotypus canaliculatum. Eur. J. Biochem. 143, 257-265. CrossRef
Samain, J.F., Dégremont, L., Soletchnik, P., Haure, J., Bédier, E., Ropert, M., Moal, J., Huvet, A., Bacca, H., Van Wormhoudt, A., et al., 2007, Genetically based resistance to summer mortality in the Pacific oyster (Crassostrea gigas) and its relationship with physiological, immunological characteristics and infection processes. Aquaculture 268, 227-243. CrossRef
Simcic, T., Brandcelj, A., 2006, Effects of pH on electron transport system (ETS) activity and oxygen consumption in Gammarus fossarum, Asellus aquaticus and Niphargus sphagnicolus. Freshwater Biol. 51, 686-694. CrossRef
Shick, J.M., Gnaiger, E., Widdows, J., Bayne, B.L., de Zwann, A., 1986, Activity and metabolism in the mussel Mytilus edulis L. during intertidal hypoxia and aerobic recovery. Physiol. Zool. 59, 627-642. CrossRef
Simpfendörfer, R.W., Vial, M.V., Monsalve, A., 1997, The adductor muscle pyruvate kinase from the intertidal bivalve Mytilus chilensis (Hupé): evidence of the presence of a phosphorylated form of the enzyme during the entire tidal cycle. J. Exp. Mar. Biol. Ecol. 213, 169-179. CrossRef
Sobral, P., Widdows, J., 1997, Influence of hypoxia and anoxia on the physiological responses of the clam Ruditapes decussatus from southern Portugal. Mar. Biol. 127, 455-461. CrossRef
Soletchnik, P., Le Moine, O., Faury, N., Razet, D., Geairon, P., Goulletquer, P., 1999, Summer mortality of the oyster in the Bay Marennes-Oléron: Spatial variability of environment and biology using a geographical information system (GIS). Aquat. Living Resour. 12, 131-143. CrossRef
Soletchnik, P., Lambert, C., Costil, K., 2005, Summer mortality of Crassostrea gigas (Thunberg) in relation to environmental rearing conditions. J. Shellfish Res. 24, 197-207.
Soletchnik, P., Faury, N., Goulletquer, P., 2006, Seasonal changes in carbohydrate metabolism and its relationship with summer mortality of Pacific oyster Crassostrea gigas (Thunberg) in Marennes-Oléron bay (France). Aquaculture 252, 328-338.
Storey K.B., 1993, Molecular mechanism of metabolic arrest in molluscs. In: Hochachka P.W., Lutz P.L., Sick T., Rosenthal M., van den Thillart G. (Eds.) Surviving Hypoxia : Mechanisms of Control and Adaptation. CRC Press; Boca Raton; pp. 253-269.
Vismann, B., 1991, Sulfide tolerance: Physiological mechanisms and ecological implications. Ophelia 34, 1-27.
Williamson D.H., 1974, Determination with alanine dehydrogenase. In: Bergmeyer H.U. (Ed.), Methods of Enzymatic Analysis. Vol. 2. Academic Press, New York, pp.1679-1682.