Journal of Comparative Physiology B

, Volume 176, Issue 5, pp 441–452 | Cite as

Food deprivation alters osmoregulatory and metabolic responses to salinity acclimation in gilthead sea bream Sparus auratus

  • Sergio Polakof
  • Francisco J. Arjona
  • Susana Sangiao-Alvarellos
  • María P. Martín del Río
  • Juan M. Mancera
  • José L. Soengas
Original Paper

Abstract

The influence of acclimation to different environmental salinities (low salinity water, LSW; seawater, SW; and hyper saline water, HSW) and feeding conditions (fed and food deprived) for 14 days was assessed on osmoregulation and energy metabolism of several tissues of gilthead sea bream Sparus auratus. Fish were randomly assigned to one of six treatments: fed fish in LSW, SW, and HSW, and food-deprived fish in LSW, SW, and HSW. After 14 days, plasma, liver, gills, kidney and brain were taken for the assessment of plasma osmolality, plasma cortisol, metabolites and the activity of several enzymes involved in energy metabolism. Food deprivation abolished or attenuated the increase in gill Na+,K+-ATPase activity observed in LSW- and HSW-acclimated fish, respectively. In addition, a linear relationship between renal Na+,K+-ATPase activity and environmental salinity was observed after food deprivation, but values decreased with respect to fed fish. Food-deprived fish acclimated to extreme salinities increased production of glucose through hepatic gluconeogenesis, and the glucose produced was apparently exported to other tissues and served to sustain plasma glucose levels. Salinity acclimation to extreme salinities enhanced activity of osmoregulatory organs, which is probably sustained by higher glucose use in fed fish but by increased use of other fuels, such as lactate and amino acids in food-deprived fish.

Keywords

Osmotic acclimation Food deprivation Gilthead sea bream Energy metabolism 

Abbreviations

Ala-AT

Alanine aminotransferase (EC. 2.6.1.2)

Asp-AT

Aspartate aminotransferase (EC. 2.6.1.1)

ELISA

Indirect enzyme immunoassay

HK

Hexokinase (EC. 2.7.1.11)

FBPase

Fructose 1,6-bisphosphatase (EC. 3.1.3.11)

FW

Freshwater

G3PDH

Glyceraldehyde 3-phosphate dehydrogenase (EC. 1.1.1.8)

G6Pase

Glucose 6-phosphatase (EC. 3.1.3.9)

G6PDH

Glucose 6-phosphate dehydrogenase (EC. 1.1.1.49)

GDH

Glutamate dehydrogenase (EC. 1.4.1.2)

GK

Glucokinase (EC. 2.7.1.2)

GPase

Glycogen phosphorylase (EC. 2.4.1.1)

HOAD

3-Hydroxiacil-CoA-dehydrogenase (EC. 1.1.1.35)

HSW

High salinity water

LDH-O

Lactate dehydrogenase-oxidase (EC. 1.1.1.27)

LSW

Low salinity water

PFK

6-Phosphofructo 1-kinase (EC. 2.7.1.11)

PK

Pyruvate kinase (EC. 2.7.1.40)

SEI

Sucrose-EDTA-imidazole

SW

Seawater

Notes

Acknowledgements

This study was partly supported by grants VEM2003-20062 (Ministerio de Ciencia y Tecnología and FEDER, Spain), and PGIDT04PXIC31208PN and PGIDIT05PXIC31202PN (Xunta de Galicia, Spain) to J.L. Soengas, and grant BFU2004-04439-CO2-01B (Ministerio de Ciencia y Tecnología and FEDER, Spain) to J.M. Mancera. The authors wish to thank Planta de Cultivos Marinos (CASEM, Universidad de Cádiz, Puerto Real, Cádiz, Spain) for providing them with experimental fish.

References

  1. Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 129:3–26CrossRefGoogle Scholar
  2. Bonamusa L, García de Frutos P, Fernández F, Baanante IV (1992) Nutritional effects on key glycolytic–gluconeogenic enzyme activities and metabolite levels in the liver of the teleost fish Sparus aurata. Mol Marine Biol Biotechnol 1:113–125Google Scholar
  3. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  4. Caseras A, Metón I, Vives C, Egea M, Fernández F, Baanante IV (2002) Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata). Br J Nutr 88:607–614CrossRefPubMedGoogle Scholar
  5. Chervinski J (1984) Salinity tolerance of young gilthead sea bream Sparus aurata. Bamidgeh 36:121–124Google Scholar
  6. Collins AL, Anderson TA (1997) The influence of changes in food availability on the activation of key degradative and metabolic enzymes in the liver and epaxial muscle of the golden Perch. J Fish Biol 50:1158–1165CrossRefGoogle Scholar
  7. Figueroa RI, Rodríguez-Sabarís R, Aldegunde M, Soengas JL (2000) Effects of food deprivation on 24 h-changes in brain and liver carbohydrate and ketone body metabolism of rainbow trout. J Fish Biol 57:631–646Google Scholar
  8. Foster GD, Moon TW (1991) Hypometabolism with fasting in the yellow perch: a study of enzymes, hepatocyte metabolism, and tissue size. Physiol Zool 64:259–275Google Scholar
  9. Guzmán JM, Sangiao-Alvarellos S, Laiz-Carrión R, Míguez JM, Martín del Rio MP, Soengas JL, Mancera JM (2004) Osmoregulatory action of 17β-estradiol in the gilthead sea bream Sparus auratus. J Exp Zool 301A:828–836CrossRefGoogle Scholar
  10. Jarvis PL, Ballantyne JS (2003) Metabolic responses to salinity acclimation in juvenile shortnose sturgeon Acipenser brevirostrum. Aquaculture 219:891–909CrossRefGoogle Scholar
  11. Jorgensen EH, Vijayan MM, Aluru N, Maule AG (2002) Fasting modifies Aroclor 1254 impact on plasma cortisol, glucose and lactate responses to handling disturbance in Arctic charr. Comp Biochem Physiol 132C:235–245Google Scholar
  12. Jürss K, Bittorf T, Vökler T (1986) Influence of salinity and food deprivation on growth, RNA/DNA ratio and certain enzyme activities in rainbow trout (Salmo gairdneri Richardson). Comp Biochem Physiol 83B:425–433Google Scholar
  13. Kelly SP, Chow INK, Woo NYS (1999) Haloplasticity of black seabream (Mylio macrocephalus): hypersaline to freshwater acclimation. J Exp Zool 283:226–241CrossRefGoogle Scholar
  14. Keppler D, Decker K (1974) Glycogen. determination with amyloglucosidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Acdemic, New York, pp 1127–1131Google Scholar
  15. Kirchner S, Seixas P, Kaushik S, Panserat S (2005) Effects of low protein intake on extra-hepatic gluconeogenic enzyme expression and peripheral glucose phosphorylation in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol 140B:333–340Google Scholar
  16. Kültz D, Jürss K (1991) Acclimation of chloride cells and Na/K-ATPase to energy deficiency in tilapia (Oreochromis mossambicus). Zool Jb Physiol 95:39–50Google Scholar
  17. Laiz-Carrión R, Sangiao-Alvarellos S, Guzmán JM, Martín del Rio MP, Soengas JL, Mancera JM (2002) Energy metabolism in fish tissues related to osmoregulation and cortisol action. Fish Physiol Biochem 27:179–188CrossRefGoogle Scholar
  18. Laiz-Carrión R, Martín del Río MP, Míguez JM, Mancera JM, Soengas JL (2003) Influence of cortisol on osmoregulation and energy metabolism in gilthead sea bream Sparus aurata. J Exp Zool 298A:105–118CrossRefGoogle Scholar
  19. Laiz-Carrión R, Guerreiro PM, Fuentes J, Canario AVM, Martín del Rio MP, Mancera JM (2005a) Branchial osmoregulatory response to salinity in the gilthead sea bream, Sparus auratus. J Exp Zool 303A:563–576CrossRefGoogle Scholar
  20. Laiz-Carrión R, Sangiao-Alvarellos S, Guzmán JM, Martín del Rio MP, Soengas JL, Mancera JM (2005b) Growth performance of gilthead sea bream Sparus aurata in different osmotic conditions: implications on osmoregulation and energy metabolism. Aquaculture 250:849–861CrossRefGoogle Scholar
  21. Mancera JM, Pérez-Fígares JM, Fernández-Llebrez P (1993a) Osmoregulatory responses to abrupt salinity changes in the euryhaline gilthead sea bream (Sparus aurata). Comp Biochem Physiol 106A:245–250CrossRefGoogle Scholar
  22. Mancera JM, Fernández-Llebrez P, Grondona JM, Pérez-Fígares JM (1993b) Influence of environmental salinity on prolactin and corticotropic cells in the euryhaline gilthead sea bream (Sparus aurata L.). Gen Comp Endocrinol 90:220–231CrossRefPubMedGoogle Scholar
  23. Mancera JM, Laiz-Carrión R, Martín del Río MP (2002) Osmoregulatory action of PRL, GH and cortisol in the gilthead sea bream (Sparus aurata L.). Gen Comp Endocrinol 129:95–103CrossRefPubMedGoogle Scholar
  24. McCormick SD (1993) Methods for nonlethal gill biopsy and measurement of Na+,K+-ATPase activity. Can J Fish Aquat Sci 50:656–658Google Scholar
  25. Metón I, Caseras A, Fernández F, Baanante IV (2004) Molecular cloning of hepatic glucose-6-phosphatase catalytic subunit from gilthead sea bream (Sparus aurata): response of its mRNA levels and glucokinase expression to refeeding and diet composition. Comp Biochem Physiol 138B:145–153Google Scholar
  26. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268CrossRefGoogle Scholar
  27. Moon TW, Foster GD, Plisetskaya EM (1989) Changes in peptide hormones and liver enzymes in the rainbow trout deprived of food for 6 weeks. Can J Zool 67:2189–2193CrossRefGoogle Scholar
  28. Moore S (1968). Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the nynhidrin reaction. J Biol Chem 1242:6281–6283Google Scholar
  29. Nakano K, Tagawa M, Takemura A, Hirano T (1997) Effects of ambient salinities on carbohydrate metabolism in two species of tilapia: Oreochromis mossambicus and O. niloticus. Fish Sci 63:338–343Google Scholar
  30. Navarro I, Gutiérrez J (1995) Fasting and starvation. In: Hochachka PW, Mommsen TP (eds) Metabolic biochemistry, biochemistry and molecular biology of fishes, vol 4. Elsevier, Amsterdam, pp 393–434Google Scholar
  31. Panserat S, Médale F, Blin C, Brèque J, Vachot C, Plagnes-Juan E, Gomes E, Krishnamoorthy R, Kaushik S (2000) Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilhead seabream, and common carp. Am J Physiol 278:R1164–R1170Google Scholar
  32. Reubush KJ, Heath AG (1996) Metabolic responses to acute handling by fingerling inland and anadromous striped bass. J Fish Biol 49:830–841CrossRefGoogle Scholar
  33. Sangiao-Alvarellos S, Laiz-Carrión R, Guzmán JM, Martín del Rio MP, Míguez JM, Mancera JM, Soengas JL (2003) Acclimation of S. aurata to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am J Physiol 285:R897–R907Google Scholar
  34. Sangiao-Alvarellos S, Lapido M, Míguez JM, Soengas JL (2004) Effects of central administration of arginine vasotocin on monoaminergic neurotransmitters and energy metabolism of rainbow trout brain. J Fish Biol 64:1313–1329CrossRefGoogle Scholar
  35. Sangiao-Alvarellos S, Guzmán JM, Laiz-Carrión R, Martín del Río MP, Míguez JM, Mancera JM, Soengas JL (2005a). 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 146:607–617CrossRefGoogle Scholar
  36. Sangiao-Alvarellos S, Guzmán JM, Laiz-Carrión R, Míguez JM, Martín del Río MP, Mancera JM, Soengas JL (2005b) Interactive effects of high stocking density and food deprivation on carbohydrate metabolism in several tissues of gilthead sea bream Sparus auratus. J Exp Zool 303A:761–775CrossRefGoogle Scholar
  37. Sangiao-Alvarellos S, Arjona FJ, Martín del Río MP, Míguez JM, Mancera JM, Soengas JL (2005c) Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus. J Exp Biol 208:4291–4304CrossRefPubMedGoogle Scholar
  38. Sheridan MA, Mommsen TP (1991) Effects of nutritional state on in vivo lipid and carbohydrate metabolism of Coho Salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 81:473–483CrossRefPubMedGoogle Scholar
  39. Soengas JL, Strong EF, Fuentes J, Veira JAR, Andrés MD (1996) Food deprivation and refeeding in Atlantic salmon, Salmo salar: effects on brain and liver carbohydrate and ketone bodies metabolism. Fish Physiol Biochem 15:491–511CrossRefGoogle Scholar
  40. Soengas JL, Strong EF, Andrés MD (1998) Glucose, lactate, and β-hydroxybutyrate utilization by rainbow trout brain: changes during food deprivation. Physiol Zool 71:285–293PubMedGoogle Scholar
  41. Sundby A, Hemre GI, Borrebaek B, Christophersen B, Blom AK (1991) Insulin and glucagon family peptides in relation to activities of hepatic hexokinase and other enzymes in fed and starved atlantic salmon (Salmo salar) and cod (Gadus morhua). Comp Biochem Physiol 100B:467–470Google Scholar
  42. Tintos A, Míguez JM, Mancera JM, Soengas JL (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)Google Scholar
  43. Tripathi G, Verma P (2003) Starvation-reduced impairment of metabolism in a freshwater catfish. Zeitschrift fur Naturforschung C 58:446–451Google Scholar
  44. Vijayan MM, Moon TW (1992) Acute handling stress alters hepatic glycogen metabolism in food-deprived rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 49:2260–2266CrossRefGoogle Scholar
  45. Vijayan MM, Morgan JD, Sakamoto T, Grau EG, Iwama GK (1996) Food-deprivation affects seawater acclimation in tilapia: hormonal and metabolic changes. J Exp Biol 199:2467–2475PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Sergio Polakof
    • 1
  • Francisco J. Arjona
    • 2
  • Susana Sangiao-Alvarellos
    • 1
  • María P. Martín del Río
    • 2
  • Juan M. Mancera
    • 2
  • José L. Soengas
    • 1
  1. 1.Laboratorio de Fisioloxía Animal, Facultade de Ciencias do Mar, Edificio de Ciencias ExperimentaisUniversidade de VigoVigoSpain
  2. 2.Departamento de Biología, Facultad de Ciencias del Mar y AmbientalesUniversidad de CádizPuerto RealSpain

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