Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus

Journal of Experimental Biology - Tập 208 Số 22 - Trang 4291-4304 - 2005
Susana Sangiao‐Alvarellos1, Francisco J. Arjona2, M.P. Martı́n del Rı́o2, Jesús M. Míguez1, Juan Miguel Mancera2, José L. Soengas1
1Laboratorio de Fisioloxía Animal, Facultade de Ciencias do Mar, Universidade de Vigo, 36310 Vigo, Spain
2Departamento de Biología, Facultad de Ciencias del Mar y Ambientales, Universidad de Cádiz, 11510 Puerto Real, Cádiz, Spain

Tóm tắt

SUMMARY Changes in different osmoregulatory and metabolic parameters over time were assessed in gills, kidney, liver and brain of gilthead sea bream Sparus auratus transferred either from seawater (SW, 38 p.p.t.) to hypersaline water (HSW, 55 p.p.t.) or from SW to low salinity water (LSW, 6 p.p.t.) for 14 days. Changes displayed by osmoregulatory parameters revealed two stages during hyperosmotic and hypo-osmotic acclimation: (i) an adaptive period during the first days of acclimation (1–3 days), with important changes in these parameters, and (ii) a chronic regulatory period (after 3 days of transfer) where osmotic parameters reached homeostasis. From a metabolic point of view, two clear phases can also be distinguished during acclimation to hyperosmotic or hypo-osmotic conditions. The first one coincides with the adaptive period and is characterized by enhanced levels of plasma metabolites(glucose, lactate, triglycerides and protein), and use of these metabolites by different tissues in processes directly or indirectly involved in osmoregulatory work. The second stage coincides with the chronic regulatory period observed for the osmoregulatory parameters and is metabolically characterized in HSW-transferred fish by lower energy expenditure and a readjustment of metabolic parameters to levels returning to normality,indicative of reduced osmoregulatory work in this stage. In LSW-transferred fish, major changes in the second stage include: (i) decreased glycolytic potential, capacity for exporting glucose and potential for amino acid catabolism in liver; (ii) enhanced use of exogenous glucose through glycolysis, pentose phosphate and glycogenesis in gills; (iii) increased glycolytic potential in kidney; and (iv) increased glycogenolytic potential and capacity for use of exogenous glucose in brain.

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Tài liệu tham khảo

Blasco, J., Marimon, I., Viaplana, I. and Fernández-Borrás, J. (2001). Fate of plasma glucose in tissues of brown trout in vivo: effects of fasting and glucose loading. Fish Physiol. Biochem.24,247-258.

Boeuf, G. and Payan, P. (2001). How should salinity influence fish growth? Comp. Biochem. Physiol.130,411-423.

Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem.72,248-254.

Chervinski, J. (1984). Salinity tolerance of young gilthead sea bream Sparus aurata.Bamidgeh.36,121-124.

De Boeck, G., Vlaeminck, A., Van der Linden, A. and Blust,R. (2000). The energy metabolism of common carp (Cyprinus carpio) when exposed to salt stress: an increase in energy expenditure or effects of starvation? Physiol. Biochem. Zool.73,102-111.

Deane, E. E. and Woo, N. Y. S. (2004). Differential gene expression associated with euryhalinity in sea bream(Sparus sarba). Am. J. Physiol.287,R1054-R1063.

Guzmán, J. M., Sangiao-Alvarellos, S.,Laiz-Carrión, R., Míguez, J. M., Martín del Rio, M. P.,Soengas, J. L. and Mancera, J. M. (2004). Osmoregulatory action of 17β-estradiol in the gilthead sea bream Sparus auratus.J. Exp. Zool.301,828-836.

Holmes, W. N. and Donaldson, E. M. (1969). The body compartments and the distribution of electrolytes. In Fish Physiology, Vol. 1 (ed. W. S. Hoar, and D. J. Randall), pp. 1-89. San Diego: Academic Press.

Jensen, M. K., Madsen, S. S. and Kristiansen, K.(1998). Osmoregulation and salinity effects on the expression and activity of Na+,K+-ATPase in the gills of european sea bass, Dicentrarchus labrax (L.). J. Exp. Zool.282,290-300.

Kelly, S. P. and Woo, N. Y. S. (1999a). Cellular and biochemical characterization of hypo-osmotic adaptation in a marine teleost, Sparus sarba.Zool. Sci.16,505-514.

Kelly, S. P. and Woo, N. Y. S. (1999b). The response of seabream following abrupt hypo-osmotic exposure. J. Exp. Biol.55,732-750.

Kelly, S. P., Chow, I. N. K. and Woo, N. Y. S.(1999). Haloplasticity of black seabream (Mylio macrocephalus): Hypersaline to freshwater acclimation. J. Exp. Zool.283,226-241.

Keppler, D. and Decker, K. (1974). Glycogen. Determination with amyloglucosidase. In Methods of Enzymatic Analysis (ed. H. U. Bergmeyer), pp.1127-1131. New York: Academic Press.

Laiz-Carrión, R., Sangiao-Alvarellos, S., Guzmán,J. M., Martín del Rio, M. P., Míguez, J. M., Soengas, J. L. and Mancera, J. M. (2002). Energy metabolism in fish tissues related to osmoregulation and cortisol action. Fish Physiol. Biochem.27,179-188.

Laiz-Carrión, R., Martín del Río, M. P.,Míguez, J. M., Mancera, J. M. and Soengas, J. L.(2003). Influence of cortisol on osmoregulation and energy metabolism in gilthead sea bream Sparus aurata.J. Exp. Zool.298,105-118.

Laiz-Carrión, R., Guerreiro, P. M., Fuentes, J., Canario,A. V. M., Martín del Rio, M. P. and Mancera, J. M.(2005a). Branchial osmoregulatory response to salinity in the gilthead sea bream, Sparus auratus.J. Exp. Zool.303,563-576.

Laiz-Carrión, R., Sangiao-Alvarllos, S., Guzmán,J. M., Martín del Río, M. P., Soengas, J. L. and Mancera, J. M. (2005b). Growth performance of gilthead sea bream Sparus aurata in different osmotic conditions: implications for osmoregulation and energy metabolism. Aquaculture. In press.

Lasserre, P. (1971). Increase of(Na++K+)dependent ATPase activity of gills and kidney of two euryhaline marine teleosts, Crenimugil labrosus (Risso, 1826) and Dicentrarchus labrax (Linnaeus, 1758), during adaptation to fresh water. Life Sci.10,113-119.

Le François, N. R., Lamarre, S. G. and Blier, P. U.(2004). Tolerance, growth and haloplasticity of the Atlantic wolfish (Anarhichas lupus) exposed to various salinities. Aquaculture236,659-675.

Lin, C. H., Tsai, R. S. and Lee, T. H. (2004). Expression and distribution of Na, K-ATPase in gill and kidney of the spotted green pufferfish, Tetraodon nigroviridis, in response to salinity challenge. Comp. Biochem. Physiol.138,287-295.

Maetz, J. (1974). Aspects of adaptation to hypo-osmotic and hyper-osmotic environments. In Biochemical and Biophysical Perspectives in Marine Biology (ed. D. C. Malins and J. R. Sargent), pp. 1-167. New York: Academic Press.

Mancera, J. M., Laiz-Carrión, R. and Martín del Río, M. P. (2002). Osmoregulatory action of PRL, GH and cortisol in the gilthead sea bream (Sparus aurata L.). Gen. Comp. Endocrinol.129,95-103.

Mancera, J. M., Pérez-Fígares, J. M. and Fernández-Llebrez, P. (1993a). Osmoregulatory responses to abrupt salinity changes in the euryhaline gilthead sea bream(Sparus aurata). Comp. Biochem. Physiol.106,245-250.

Mancera, J. M., Fernández-Llebrez, P., Grondona, J. M. and Pérez-Fígares, J. M. (1993b). Influence of environmental salinity on prolactin and corticotropic cells in the euryhaline gilthead sea bream (Sparus aurata L.). Gen. Comp. Endocrinol.90,220-231.

Mancera, J. M., Pérez-Fígares, J. M. and Fernández-Llebrez, P. (1994). Effect of cortisol on brackish water adaptation in the euryhaline gilthead sea bream (Sparus aurata L.). Comp. Biochem. Physiol.107,397-402.

Mancera, J. M., Pérez-Fígares, J. M. and Fernández-Llebrez, P. (1995). Effect of decreased environmental salinity on growth hormone cells in the euryhaline gilthead sea bream (Sparus aurata L.). J. Fish Biol.46,494-500.

Marshall, W. S. (2002). Na+,Cl-, Ca2+ and Zn2+ transport by fish gills:retrospective review and prospectives synthesis. J. Exp. Zool.293,264-283.

Marshall, W. S., Emberley, T. R., Singer, T. D., Bryson, S. E. and McCormick, S. D. (1999). Time course of salinity adaptation in a strongly euryhaline estuarine teleost, Fundulus heteroclitus: a multivariable approach. J. Exp. Biol.202,1535-1544.

McCormick, S. D. (1993). Methods for nonlethal gill biopsy and measurement of Na+,K+-ATPase activity. Can. J. Fish. Aquat. Sci.50,656-658.

McCormick, S. D. (1995). Hormonal control of gill Na+,K+-ATPase and chloride cell function. In Fish Physiology, Vol. 14 (ed. C. M. Wood and T. J. Shuttleworth), pp. 285-315. San Diego: Academic Press.

McCormick, S. D. (2001). Endocrine control of osmoregulation in teleost fish. Am. Zool.41,781-794.

Mommsen, T. P. (1984). Metabolism of the fish gill. In Fish Physiology, VolXB (ed. W. S. Hoar and D. J. Randall), pp.203-238. New York: Academic Press.

Mommsen, T. P., Walsh, P. J. and Moon, T. W.(1985). Gluconeogenesis in hepatocytes and kidney of Atlantic salmon. Mol. Physiol.8,89-100.

Mommsen, T. P., Vijayan, M. M. and Moon, T. W.(1999). Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation Rev.Fish Biol. Fish.9, 211-268.

Morgan, J. D. and Iwama, G. K. (1991). Effects of salinity on growth, metabolism, and ion regulation in juvenile rainbow trout (Oncorhynchus mykiss) and fall Chinook salmon (Oncorhynchus tshawytscha). Can. J. Fish. Aquat. Sci.48,2083-2094.

Morgan, J. D., Sakamoto, T., Grau, E. G. and Iwama, G. K.(1997). Physiological and respiratory responses of the Mozambique tilapia (Oreochromis mossambicus) to salinity acclimation. Comp. Biochem. Physiol.117,391-398.

Nakano, K., Tagawa, M., Takemura, A. and Hirano, T.(1997). Effects of ambient salinities on carbohydrate metabolism in two species of tilapia: Oreochromis mossambicus and O. niloticus.Fish. Sci.63,338-343.

Nakano, K., Tagawa, M., Takemura, A. and Hirano, T.(1998). Temporal changes in liver carbohydrate metabolism associated with seawater transfer in Oreochromis mossambicus.Comp. Biochem. Physiol.119,721-728.

Nordgarden, U., Hemre, G. I. and Hansen, T.(2002). Growth and body composition of Atlantic salmon (Salmo salar L.) parr and smolt fed diets varying in protein and lipid contents. Aquaculture207,65-78.

Richards, J. G., Semple, J. W., Bystriansky, J. S. and Schulte,P. M. (2003). Na+/K+-ATPaseα-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J. Exp. Biol.206,4475-4486.

Roche, H., Chaar, K. and Pérès, G.(1989). The effect of a gradual decrease in salinity on the significant constituents of tissue in the sea bass (Dicentrarchus labrax, Pisces). Comp. Biochem. Physiol.93,785-789.

Rush, J. W. E. and Spriet, L. L. (2001). Skeletal muscle glycogen phosphorylase a kinetics: effects of adenine nucleotides and caffeine. J. Appl. Physiol.91,2071-2078.

Sangiao-Alvarellos, S., Laiz-Carrión, R., Guzmán,J. M., Martín del Río, M. P., Míguez, J. M., Mancera, J. M. and Soengas, J. L. (2003). Acclimation of Sparus aurata to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am. J. Physiol.285,R897-R907.

Sangiao-Alvarellos, S., Lapido, M., Míguez, J. M. and Soengas, J. L. (2004). Effects of central administration of arginine vasotocin on monoaminergic neurotransmitters and energy metabolism of rainbow trout brain. J. Fish Biol.64,1313-1329.

Sangiao-Alvarellos, S., Míguez, J. M. and Soengas, J. L. (2005a). Actions of growth hormone on carbohydrate metabolism and osmoregulation of rainbow trout. Gen. Comp. Endocrinol.141,214-225.

Sangiao-Alvarellos, S., Guzmán, J. M.,Laiz-Carrión, R., Martín del Río, M. P., Míguez,J. M., Mancera, J. M. and Soengas, J. L. (2005b). Actions of 17β-estradiol on carbohydrate metabolism in liver, gills and brain of gilthead sea bream Sparus auratus during acclimation to different salinities. Marine Biol.146,607-617.

Scott, G. R., Richards, J. G., Forbush, B., Isenring, P. and Schulte, P. M. (2004). Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after abrupt salinity transfer. Am. J. Physiol.287,C300-C309.

Soengas, J. L. and Aldegunde, M. (2002). Energy metabolism of fish brain. Comp. Biochem. Physiol.131,271-296.

Soengas, J. L., Barciela, P., Fuentes, J., Otero, J.,Andrés, M. D. and Aldegunde, M. (1993). The effect of seawater transfer in liver carbohydrate metabolim of domesticated rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol.105,337-343.

Soengas, J. L., Fuentes, J., Andrés, M. D. and Aldegunde,M. (1994). Direct transfer of rainbow trout to seawater induces several changes in kidney carbohydrate metabolism. J. Physiol. Biochem.50,219-228.

Soengas, J. L., Aldegunde, M. and Andrés, M. D.(1995a). Gradual transfer to seawater of rainbow trout: effects on liver carbohydrate metabolism. J. Fish Biol.47,466-478.

Soengas, J. L., Barciela, P., Aldegunde, M. and Andrés,M. D. (1995b). Gill carbohydrate metabolism of rainbow trout is modified during gradual adaptation to sea water. J. Fish Biol.46,845-856.

Soengas, J. L., Strong, E. F. and Andrés, M. D.(1998). Glucose, lactate, and β-hydroxybutyrate utilization by rainbow trout brain: changes during food deprivation. Physiol. Zool.71,285-293.

Tintos, A., Míguez, J. M., Mancera, J. M. and Soengas, J. L. (2005). Development of a microtitre plate indirect ELISA for measuring cortisol in teleost fish, and evaluation of stress responses in rainbow trout and gilthead sea bream. J. Fish Biol. In press.

Venturini, G., Cataldi, E., Marino, G., Pucci, P., Garibaldi, L. and Bronz, P. (1992). Serum ions concentration and ATPase activity in gills, kidney and oesophagus of European sea bass(Dicentrarchus labrax, Pisces, Perciformes) during acclimation trial to fresh water. Comp. Biochem. Physiol.103,451-454.

Vijayan, M. M., Morgan, J. D., Sakamoto, T., Grau, E. G. and Iwama, G. K. (1996). Food-deprivation affects seawater acclimation in tilapia: hormonal and metabolic changes. J. Exp. Biol.199,2467-2475.

Weng, C. F., Chiang, C. C., Gong, H. Y., Chen, M. H. C., Huang,W. T., Cheng, C. Y. and Wu, J. L. (2002). Bioenergetics of adaptation to a salinity transition in euryhaline teleost (Oreochromis mossambicus) brain. Exp. Biol. Med.227, 45-50.

Woo, N. Y. S. and Fung, J. C. (1981). Studies on the biology of the red sea bream Chrysophrys major II. Salinity adaptation. Comp. Biochem. Physiol.69,237-242.

Woo, N. Y. S. and Murat, J. C. (1981). Studies on the biology of the red sea bream Chrysophrys major III. Metabolic response to starvation in different salinities. Marine Biol.61,255-260.

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Journal of Experimental Biology

Tập 208 Số 22

4291-4304

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