Skip to main content
Log in

Different environmental temperatures affect amino acid metabolism in the eurytherm teleost Senegalese sole (Solea senegalensis Kaup, 1858) as indicated by changes in plasma metabolites

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Senegalese sole (Solea senegalensis) is a eurytherm teleost that under natural conditions can be exposed to annual water temperature fluctuations between 12 and 26°C. This study assessed the effects of temperature on sole metabolic status, in particular in what concerns plasma free amino acid changes during thermal acclimation. Senegalese sole maintained at 18°C were acclimated to either cold (12°C) or warm (26°C) environmental temperatures for 21 days. Fish maintained at 18°C served as control. Plasma concentrations of cortisol, glucose, lactate, triglycerides, proteins, and free amino acids were assessed. Cold acclimation influenced interrenal responses of sole by increasing cortisol release. Moreover, plasma glucose and lactate concentrations increased linearly with temperature, presumably reflecting a higher metabolic activity of sole acclimated to 26°C. Acclimation temperature affected more drastically plasma concentrations of dispensable than that of indispensable amino acids, and different acclimation temperatures induced different responses. Asparagine, glutamine and ornithine seem to be of particular importance for ammonia detoxification mechanisms, synthesis of triglycerides that may be used during homeoviscous adaptation and, to a lesser extent, as energetic substrates in specimens acclimated to 12°C. When sole is acclimated to 26°C taurine, glutamate, GABA and glycine increased, which may suggest important roles as antioxidant defences, in osmoregulatory processes and/or for energetic purposes at this thermal regimen. In conclusion, acclimation to different environmental temperatures induces several metabolic changes in Senegalese sole, suggesting that amino acids may be important for thermal acclimation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268

    Article  Google Scholar 

  • Aragão C, Costas B, Vargas-Chacoff L, Ruiz-Jarabo I, Dinis MT, Mancera JM, Conceição LEC (2010) Changes in plasma amino acid levels in a euryhaline fish exposed to different environmental salinities. Amino Acids 38:311–317

    Article  PubMed  Google Scholar 

  • Arends RJ, van der Gaag R, Martens GJM, Wendelaar Bonga SE, Flik G (1998) Differential expression of two pro-opiomelanocortin mRNAs during temperature stress in common carp (Cyprinus carpio L.). J Endocrinol 159:85–91

    Article  PubMed  CAS  Google Scholar 

  • Arends RJ, Mancera JM, Muñoz JL, Wendelaar Bonga SE, Flik G (1999) The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J Endocr 163:149–157

    Article  PubMed  CAS  Google Scholar 

  • Arjona FJ, Ruiz-Jarabo I, Vargas-Chacoff L, Martín del Río MP, Flik G, Mancera JM, Klaren PHM (2010) Acclimation of Solea senegalensis to different ambient temperatures: implications for thyroidal status and osmoregulation. Mar Biol 157:1325–1335

    Article  CAS  Google Scholar 

  • Babu GR, Reddy GR, Chetty CS (1989) Perturbations in nitrogen metabolism of brain and liver of rat following repeated benthiocarb administration. Biochem Int 8:1253–1268

    Google Scholar 

  • Ballantyne JS (2001) Amino acid metabolism. In: Wright PA, Anderson PM (eds) Nitrogen excretion. Fish physiology, vol 20. Academic Press, San Diego, pp 77–107

  • Beckman BR, Larsen DA, Sharpe C, Lee-Pawlak B, Schreck CB, Dickhoff WW (2000) Physiological status of naturally reared juvenile spring chinook salmon in the Yakima River: seasonal dynamics and changes associated with smolting. Trans Am Fish Soc 129:727–753

    Article  Google Scholar 

  • Brosnan JT (2000) Glutamate, at the interface between amino acid and carbohydrate metabolism. J Nutr 130:988S–990S

    PubMed  CAS  Google Scholar 

  • Campbell CM, Davies PS (1975) Thermal acclimation in the teleost, Blennius pholis (L). Comp Biochem Physiol A 52:147–151

    Article  PubMed  CAS  Google Scholar 

  • Choi CY, Min BH, Jo PG, Chang YJ (2007) Molecular cloning of PEPCK and stress response of black porgy (Acanthopagrus schlegeli) to increased temperature in freshwater and seawater. Gen Comp Endocrinol 152:47–53

    Article  PubMed  CAS  Google Scholar 

  • Cohen SA, Meys M, Tarvin TL (1989) The Pico-Tag method—a manual of advanced techniques for amino acids analysis. Waters, Bedford

  • Cossins AR, Schwarzbaum PJ, Wieser W (1995) Effects of temperature on cellular ion regulation and membrane transport systems. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 5. Elsevier, Amsterdam, pp 101–126

  • Costas B, Aragão C, Mancera JM, Dinis MT, Conceição LEC (2008) High stocking density induces crowding stress and affects amino acid metabolism in Senegalese sole Solea senegalensis (Kaup 1858) juveniles. Aquac Res 39:1–9

    Article  CAS  Google Scholar 

  • Costas B, Aragão C, Ruiz-Jarabo I, Vargas-Chacoff L, Arjona FJ, Dinis MT, Mancera JM, Conceição LEC (2011a) Feed deprivation in Senegalese sole (Solea senegalensis Kaup, 1858) juveniles: effects on blood plasma metabolites and free amino acid levels. Fish Physiol Biochem 37:495–504

    Google Scholar 

  • Costas B, Conceição LEC, Aragão C, Martos JA, Ruiz-Jarabo I, Mancera JM, Afonso A (2011b) Physiological responses of Senegalese sole (Solea senegalensis Kaup, 1858) after stress challenge: effects on non-specific immune parameters, plasma free amino acids and energy metabolism. Aquaculture 316:68–76

    Google Scholar 

  • Couto A, Enes P, Peres H, Oliva-Teles A (2008) Effect of water and dietary starch on growth and metabolic utilization of diets in gilthead sea bream (Sparus aurata) juveniles. Comp Biochem Physiol A 151:45–50

    Article  CAS  Google Scholar 

  • De Boeck G, Nilsson GE, Vlaeminck A, Blust R (1996) Central monoaminergic responses to salinity and temperature rises in common carp. J Exp Biol 199:1605–1611

    PubMed  Google Scholar 

  • Dinis MT, Ribeiro L, Soares F, Sarasquete C (1999) A review on the cultivation potential of Solea senegalensis in Portugal and Spain. Aquaculture 176:27–38

    Article  Google Scholar 

  • Fang YZ, Yang S, Wu G (2002) Free radicals, antioxidants and nutrition. Nutrition 18:872–879

    Article  PubMed  CAS  Google Scholar 

  • Fiess JC, Kunkel-Patterson A, Mathias L, Riley LG, Yancey PH, Hirano T, Grau EG (2007) Effects of environmental salinity and temperature on osmoregulatory ability, organic osmolytes, and plasma hormone profiles in the Mozambique tilapia (Oreochromis mossambicus). Comp Biochem Physiol A 146:252–264

    Article  Google Scholar 

  • Gallardo MA, Sala-Rabanal M, Ibarz A, Padrós F, Blasco J, Fernandez-Borràs J, Sánchez J (2003) Functional alterations associated with “winter syndrome” in gilthead sea bream (Sparus aurata). Aquaculture 223:15–27

    Article  CAS  Google Scholar 

  • Goldspink G (1995) Adaptation of fish to different environmental temperature by qualitative and quantitative changes in gene expression. J Therm Biol 20:167–174

    Article  CAS  Google Scholar 

  • Hazel JR (1997) Thermal adaptation in biological membranes: beyond homeoviscous adaptation. In: Bittar EE, Willis JS (eds) Thermobiology. Advances in molecular and cell biology, vol 19. Elsevier, Amsterdam, pp 57–101

  • Ibarz A, Blasco J, Beltrán M, Gallardo MA, Sánchez J, Sala R, Fernández-Borràs J (2005) Cold-induced alterations on proximate composition and fatty acid profiles of several tissues in gilthead sea bream (Sparus aurata). Aquaculture 249:477–486

    Article  CAS  Google Scholar 

  • Ibarz A, Beltrán M, Fernández-Borràs J, Gallardo MA, Sánchez J, Blasco J (2007) Alterations in lipid metabolism and use of energy depots of gilthead sea bream (Sparus aurata) at low temperatures. Aquaculture 262:470–480

    Article  CAS  Google Scholar 

  • Imsland AK, Foss A, Conceição LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P (2003a) A review of the culture potential of Solea solea and Solea senegalensis. Rev Fish Biol Fish 13:379–407

    Article  Google Scholar 

  • Imsland AK, Gunnarsson S, Foss A, Stefansson SO (2003b) Gill Na+, K+-ATPase activity, plasma chloride and osmolality in juvenile turbot (Scophthalmus maximus) reared at different temperatures and salinities. Aquaculture 218:671–683

    Article  CAS  Google Scholar 

  • Ip YK, Chew SF, Randall DJ (2001) Ammonia toxicity, tolerance, and excretion. In: Wright PA, Anderson PM (eds) Nitrogen excretion. Fish physiology, vol 20. Academic Press, San Diego, pp 109–148

  • Johnston IA, Dunn J (1987) Temperature acclimation and metabolism in ectotherms with particular reference to teleost fish. Symp Soc Exp Biol 41:67–93

    PubMed  CAS  Google Scholar 

  • Jürss K (1979) Effects of temperature, salinity, and feeding on aminotransferase activity in the liver and white muscle of rainbow trout (Salmo gairdneri Richardson). Comp Biochem Physiol B 64:213–218

    Article  PubMed  Google Scholar 

  • Jürss K, Bastrop R (1995) Amino acid metabolism in fish. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 4. Elsevier, Amsterdam, pp 159–189

  • Lalouette L, Koštál V, Colinet H, Gagneul D, Renault D (2007) Cold exposure and associated metabolic changes in adult tropical beetles exposed to fluctuating thermal regimes. FEBS J 274:1759–1767

    Article  PubMed  CAS  Google Scholar 

  • Lankford SE, Adams TE, Cech JJ (2003) Time of day and water temperature modify the physiological stress response in green sturgeon, Acipenser medirostris. Comp Biochem Physiol A 135:291–302

    Article  CAS  Google Scholar 

  • Larsen DA, Beckman BR, Dickhoff WW (2001) The effect of low temperature and fasting during the winter on metabolic stores and endocrine physiology (insulin, insulin-like growth factor-I, and thyroxine) of coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 123:308–323

    Article  PubMed  CAS  Google Scholar 

  • Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino acids 37:43–53

    Article  PubMed  Google Scholar 

  • Mancera JM, Vargas-Chacoff L, García-López A, Kleszczyńska A, Kalamarz H, Martínez-Rodríguez G, Kulczykowska E (2008) High density and food deprivation affect arginine vasotocin, isotocin and melatonin in gilthead sea bream (Sparus aurata). Comp Biochem Physiol A 149:92–97

    Article  Google Scholar 

  • McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15

    Article  PubMed  Google Scholar 

  • Metz JR, van den Burg EH, Wendelaar Bonga SE, Flik G (2003) Regulation of branchial Na+/K+-ATPase in common carp Cyprinus carpio L. acclimated to different temperatures. J Exp Biol 206:2273–2280

    Article  PubMed  CAS  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268

    Article  Google Scholar 

  • Nye C, Kim J, Kalhan SC, Hanson RW (2008) Reassessing triglyceride synthesis in adipose tissue. Trends Endocrin Met 19:356–361

    Article  CAS  Google Scholar 

  • Parihar MS, Javeri T, Hemnani T, Dubey AK, Prakash P (1997) Responses of superoxide dismutase, glutathione peroxidase and reduced glutathione antioxidant defenses in gills of the freshwater catfish (Heteropneustes fossills) to short-term elevated temperature. J Therm Biol 22:151–156

    Article  CAS  Google Scholar 

  • Pinto W, Aragão C, Soares F, Dinis MT, Conceição LEC (2007) Growth, stress response and free amino acid levels in Senegalese sole (Solea senegalensis Kaup 1858) chronically exposed to exogenous ammonia. Aquac Res 38:1198–1204

    Article  CAS  Google Scholar 

  • Polakof S, Arjona FJ, Sangiao-Alvarellos S, Míguez JM, Martín del Río MP, Mancera JM, Soengas JL (2006) Food deprivation alters osmoregulatory and metabolic responses to salinity acclimation in gilthead sea bream Sparus aurata. J Comp Physiol B 176:441–452

    Article  PubMed  Google Scholar 

  • Pörtner HO, Lucassen M, Storch D (2005) Metabolic biochemistry: its role in thermal tolerance and in the capacities of physiological and ecological function. In: Farrell AP, Steffensen JF (eds) The physiology of polar fishes. Fish physiology, vol 22. Academic Press, San Diego, pp 79–154

  • Portz DE, Woodley CM, Cech JJ (2006) Stress-associated impacts of short-term holding of fishes. Rev Fish Biol Fisher 16:125–170

    Article  Google Scholar 

  • Randall DJ, Tsui TKN (2002) Ammonia toxicity in fish. Mar Pollut Bull 45:17–23

    Article  PubMed  CAS  Google Scholar 

  • Rotllant J, Ruane NM, Dinis MT, Canário AVM, Power DM (2006) Intra-adrenal interactions in fish: Catecholamine stimulated cortisol release in sea bass (Dicentrarchus labrax L.). Comp Biochem Physiol A 143:375–381

    Article  Google Scholar 

  • Sebert P, Barthelemy L, Caroff J (1985) Serotonin levels in fish brain: effects of hydrostatic pressure and water temperature. Experientia 41:1429–1430

    Article  CAS  Google Scholar 

  • 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 15:491–511

    Article  CAS  Google Scholar 

  • Somero GN (2004) Adaptation of enzymes to temperature: searching for basic strategies. Comp Biochem Physiol B 139:321–333

    Article  PubMed  Google Scholar 

  • Squires EJ, Hall DE, Feltham LAW (1979) Seasonal changes in plasma amino acid levels in the winter flounder (Pseudopleuronectes americanus). Can J Zool 57:1438–1442

    Article  CAS  Google Scholar 

  • Stevens ED, Sutterlin AM (1976) Heat transfer between fish and ambient water. J Exp Biol 65:131–145

    PubMed  CAS  Google Scholar 

  • Tsai CL, Wang LH (1997) Effects of thermal acclimation on the neurotransmitters, serotonin and norepinephrine in the discrete brain of male and female tilapia, Oreochromis mossambicus. Neurosci Lett 233:77–80

    Article  PubMed  CAS  Google Scholar 

  • Tsai CL, Wang LH, Tsai CC (2002) Role of serotonin, γ-aminobutyric acid, and glutamate in the behavioral thermoregulation of female tilapia during the prespawning phase. J Exp Zool 293:443–449

    Article  PubMed  CAS  Google Scholar 

  • Vargas-Chacoff L, Arjona FJ, Ruiz-Jarabo I, Páscoa I, Gonçalves O, Martín del Río MP, Mancera JM (2009a) Seasonal variation in osmoregulatory and metabolic parameters in earthen pond cultured gilthead sea bream Sparus auratus. Aquac Res 40:1279–1290

    Article  CAS  Google Scholar 

  • Vargas-Chacoff L, Arjona FJ, Polakof S, Martín del Río MP, Soengas JL, Mancera JM (2009b) Interactive effects of environmental salinity and temperature on metabolic responses of gilthead sea bream Sparus aurata. Comp Biochem Physiol A 154:417–424

    Article  Google Scholar 

  • Vinagre C, Fonseca V, Cabral H, Costa MJ (2006) Habitat suitability index models for the juveniles soles, Solea solea and Solea senegalensis, in the Tagus estuary: defining variables for species management. Fish Res 82:140–149

    Article  Google Scholar 

  • Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 7:591–625

    Google Scholar 

  • Woo NYS (1990) Metabolic and osmoregulatory changes during temperature acclimation in the red sea bream, Chrysophrys major: implications for its culture in the subtropics. Aquaculture 87:197–208

    Article  Google Scholar 

  • Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by projects STRESSAA–POCTI/CVT/49324/2002 (FCT, Portugal and FEDER), AGL2007-61211/ACU (Ministerio de Educación y Ciencia, Spain) and Proyecto de Excelencia PO7-RNM-02843 (Consejería de Innovación, Ciencia y Empresa. Junta de Andalucía) to J.M.M. Benjamín Costas and Cláudia Aragão were supported by Fundação para a Ciência e Tecnologia, Portugal (SFRH/BD/38697/2007 and SFRH/BPD/37197/2007, respectively). The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Benjamín Costas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Costas, B., Aragão, C., Ruiz-Jarabo, I. et al. Different environmental temperatures affect amino acid metabolism in the eurytherm teleost Senegalese sole (Solea senegalensis Kaup, 1858) as indicated by changes in plasma metabolites. Amino Acids 43, 327–335 (2012). https://doi.org/10.1007/s00726-011-1082-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-011-1082-0

Keywords

Navigation