Abstract
Surrounding environmental temperatures affect many aspects of ectotherm physiology. Generally, organisms can compensate at one or more biological levels, or allow temperature to dictate processes such as enzyme activities through kinetic effects on reaction rates. As digestion also alters physiological processes such as enzyme activities, this study determined the interacting effect of thermal acclimation (8 and 20 °C) and digesting a single meal on maximal enzyme activities in three tissues of the goldfish (Carrassius auratus). Acclimation to elevated temperatures decreased branchial Na+, K+, ATPase (NKA) activity. In contrast, acclimation to elevated temperatures had no effect on citrate synthase (CS) or pyruvate kinase (PK) activity in any tissue, nor were renal NKA or glutamine synthetase (GS) activities impacted. Warm water-acclimation exaggerated the positive impact of digestion on intestinal and branchial NKA activities and intestinal GS activity only, but digestion had no effect in the kidney. CS and PK did not display intestinal zonation; however, there was a distinct increase towards the distal intestine in NKA and GS activities. Zonation of NKA was more prominent in warm-acclimated animals, while acclimation temperature did not affect intestinal heterogeneity of GS. Finally, the impact of tissue protein content on enzyme activity was discussed. We conclude that the intestine and gill of warm-acclimated goldfish exhibited an augmented capacity for increasing several enzyme activities in response to digestion while the kidney was unaffected by thermal acclimation or digesting a single meal. However, this amplified capacity was ameliorated by alterations in tissue protein content. Amplified increases in NKA activity may ultimately have implications for ATP demand in these tissues, while increased GS activity may beneficially increase ammonia-detoxifying capacity in the intestine.
Similar content being viewed by others
References
Abbas G, Siddiqui PJ (2009) Effects of different feeding level on the growth, feed efficiency and body composition of juvenile mangrove red snapper, Lutjanus argentimaculatus (Forsskal 1775). Aquacult Res 40:781–789
Ahmad T, Singh SP, Khangembam BK, Sharma JG, Chakrabarti R (2014) Food consumption and digestive enzyme activity of Clarias batrachus exposed to various temperatures. Aquacult Nutr 20:265–272
Almansa E, Sanchez JJ, Cozzi S, Casariego M, Cejas J, Diaz M (2001) Segmental heterogeneity in the biochemical properties of the Na+–K+-ATPase along the intestine of the gilthead seabream (Sparus aurata L.). J Comp Physiol B 171:557–567
Baumgarner BL, Riley CP, Sepulveda MS, Brown PB, Meyer JL, Adamec J (2012) Increased expression of GAPDH protein is not indicative of nitrosative stress or apoptosis in liver of starved rainbow trout Oncorhynchus mykiss. Fish Physiol Biochem 38:319–327
Baumgarner BL, Bharadwaj AS, Inerowicz D, Goodman AS, Brown PB (2013) Proteomic analysis of rainbow trout (Oncorhynchus mykiss) intestinal epithelia: physiological acclimation to short-term starvation. Comp Biochem Physiol D 8:58–64
Bélanger F, Blier PU, Dutil JD (2002) Digestive capacity and compensatory growth in Atlantic cod (Gadus morhua). Fish Physiol Biochem 26:121–128
Bernreuther M, Herrmann JP, Peck MA, Temming A (2013) Growth energetics of juvenile herring, Clupea harengus L.: food conversion efficiency and temperature dependency of metabolic rate. J Appl Ichthyol 29:331–340
Biro PA, Post JR, Booth DJ (2007) Mechanisms for climate-induced mortality of fish populations in whole-lake experiments. Proc Natl Acad Sci 104:9715–9719
Bolinger MT, Rodnick KJ (2014) Differential effects of temperature and glucose on glycogenolytic enzymes in tissues of rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B 171:26–33
Bremer K, Moyes CD (2011) Origins of variation in muscle cytochrome c oxidase activity within and between fish species. J Exp Biol 214:1888–1895
Broer S (2008) Amino acid transport across mammalian intestinal and renal epithelia. Physiol Rev 88:249–286
Bucking C (2017) A broader look at ammonia production, excretion, and transport in fish: a review of impacts of feeding and the environment. J Comp Physiol B 187(1):1–18
Bucking C, Wood CM (2006) Gastrointestinal processing of Na+, Cl–, and K+ during digestion: implications for homeostatic balance in freshwater rainbow trout. Am J Physiol 291:R1764–R1772
Bucking C, Wood CM (2007) Gastrointestinal transport of Ca2+ and Mg2+ during the digestion of a single meal in the freshwater rainbow trout. J Comp Physiol B 177:349–360
Bucking C, Wood CM (2012) Digestion of a single meal affects gene expression of ion and ammonia transporters and glutamine synthetase activity in the intestinal tract of freshwater rainbow trout. J Comp Physiol B 182:341–350
Bucking C, Landman MJ, Wood CM (2010) The role of the kidney in compensating the alkaline tide, electrolyte load, and fluid balance disturbance associated with feeding in the freshwater rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol A 156:74–83
Bucking C, LeMoine CM, Craig PM, Walsh PJ (2013) Nitrogen metabolism of the intestine during digestion in a teleost fish, the plainfin midshipman (Porichthys notatus). J Exp Biol 216:2821–2832
Buentello JA, Gatlin DM, Neill WH (2000) Effects of water temperature and dissolved oxygen on daily feed consumption, feed utilization and growth of channel catfish (Ictalurus punctatus). Aquaculture 182:339–352
Caceci T (1984) Scanning electron microscopy of goldfish, Carassius auratus, intestinal mucosa. J Fish Biol 25:1–12
Cant JP, McBride BW, Croom WJ (1996) The regulation of intestinal metabolism and its impact on whole animal energetics. J Anim Sci 74:2541–2553
Catlett RH, Millich DR (1976) Intracellular and extracellular osmoregulation of temperature acclimated goldfish: Carassius auratus L. Comp Biochem Physiol B 55:261–269
Cossins AR (1977) Adaptation of biological membranes to temperature: the effect of temperature acclimation of goldfish upon the viscosity of synaptosomal membranes. Biochim Biophys Acta 470:395–411
Driedzic WR (1992) Cardiac energy metabolism. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish Physiology, vol XIIA. Academic, New York, pp 210–266
Enes P, Panserat S, Kaushik S, Oliva-Teles A (2006) Rapid metabolic adaptation in European sea bass (Dicentrarchus labrax) juveniles fed different carbohydrate sources after heat shock stress. Comp Biochem Physiol 145:73–81
Enes P, Panserat S, Kaushik S, Oliva-Teles A (2008) Hepatic glucokinase and glucose-6-phosphatase responses to dietary glucose and starch in gilthead sea bream (Sparus aurata) juveniles reared at two temperatures. Comp Biochem Physiol 149:80–86
Frisk M, Steffensen JF, Skov PV (2013) The effects of temperature on specific dynamic action and ammonia excretion in pikeperch (Sander lucioperca). Aquaculture 405:65–70
Furné M, Hidalgo MC, López A, García-Gallego M, Morales AE, Domezain A, Domezain J, Sanz A (2008) Effect of starvation and refeeding on digestive enzyme activities in sturgeon (Acipenser naccarii) and trout (Oncorhynchus mykiss). Comp Biochem Physiol A 149:420–425
Gao G, Moyes CD (2016) Evaluating the role of NRF-1 in the regulation of COX4-1 gene in response to temperature. J Exp Biol 219:3019–3027
German DP, Neuberger DT, Callahan MN, Lizardo NR, Evans DH (2010) Feast to famine: the effects of food quality and quantity on the gut structure and function of a detritivorous catfish (Teleostei: Loricariidae). Comp Biochem Physiol A 155:281–293
Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251
Groot JA, Albus H, Bakker R, Dekker K (1983) Changes in sugar transport and in electrophysiological characteristics of intestinal preparations of temperature-acclimated goldfish (Carassius auratus L.). J Comp Physiol 151:163–170
Guderley H (2004) Metabolic responses to low temperature in fish muscle. Biol Rev Camb Philos Soc 79:409–427
Hall KC, Bellwood DR (1995) Histological effects of cyanide, stress and starvation on the intestinal mucosa of Pomacentrus coelestis, a marine aquarium fish species. J Fish Biol 47:438–454
Hardewig I, van Dijk PLM, Leary SC, Moyes CD (2000) Temporal changes in enzyme activity and mRNA levels during thermal challenge in white sucker. J Fish Biol 56:196–207
Harpaz S, Hakim Y, Slosman T, Eroldogan OT (2005a) Effects of adding salt to the diet of Asian sea bass Lates calcarifer reared in fresh or salt water recirculating tanks, on growth and brush border enzyme activity. Aquaculture 248:315–324
Harpaz S, Hakim Y, Barki A, Karplus I, Slosman T, Tufan EO (2005b) Effects of different feeding levels during day and/or night on growth and brush-border enzyme activity in juvenile Lates calcarifer reared in freshwater re-circulating tanks. Aquaculture 248:325–335
Hayes J, Volkoff H (2014) Characterization of the endocrine, digestive and morphological adjustments of the intestine in response to food deprivation and torpor in cunner, Tautogolabrus adspersus. Comp Biochem Physiol 170:46–59
Hazel JR (1972) The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus L.)—I. Properties of the enzyme and the effect of lipid extraction. Comp Biochem Physiol 43B:338–861
Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York
Houlihan DF, Hall SJ, Gray C, Noble BS (1988) Growth rates and protein turnover in Atlantic cod, Gadus morhua. Can J Fish Aquat Sci 45(6):951–964
Jürss K, Bittorf T, Vökler T, Wacke R (1987) Effects of temperature, food deprivation and salinity on growth, RNA/DNA ratio and certain enzyme activities in rainbow trout (Salmo gairdneri Richardson). Comp Biochem Physiol 87:241–253
Kinsey ST, Locke BR, Dillaman RM (2011) Molecules in motion: influences of diffusion on metabolic structure and function in skeletal muscle. J Exp Biol 214:263–274
Kitchin SE, Morris D (1971) The effect of acclimation temperature on amino acid transport in the goldfish intestine. Comp Biochem Physiol 40:431–443
Krogdahl A, Bakke-McKellep AM (2005) Fasting and refeeding cause rapid changes in intestinal tissue mass and digestive enzyme capacities of Atlantic salmon (Salmo salar L.). Comp Biochem Physiol A 141:450–460
Kuz’mina VV, Gelman AG (1997) Membrane-linked digestion in fish. Rev Fish Sci 5:99–129
Luo Y, Xie X (2009) The effect of temperature on post-feeding ammonia excretion and oxygen consumption in the southern catfish. J Comp Physiol 179:681–689
Mackay WC (1974) Effect of temperature on osmotic and ionic regulation in goldfish, Carassius auratus L. J Comp Physiol 88:1–9
Maetz J (1972) Branchial sodium exchange and ammonia excretion in the goldfish Carassius auratus. Effects of ammonia-loading and temperature changes. J Exp Biol 56:601–620
McClelland GB, Craig PM, Dhekney K, Dipardo S (2006) Temperature and exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J Physiol 577:739–751
McCormick SD (1993) Methods for the nonlethal gill biopsy and measurements of Na+, K+-ATPase activity. Can J Fish Aquat Sci 50:656–658
McDonough AA, Farley RA (1993) Regulation of Na, K-ATPase activity. Curr Opin Nephrol Hypertens 2:725–734
McMillan DN, Houlihan DF (1989) Short-term responses of protein-synthesis to re-feeding in rainbow-trout. Aquaculture 79:37–46
Mommsen TP (1984) Biochemical characterization of the rainbow trout gill. J Comp Physiol B 154:191–198
Mommsen TP, French CJ, Hochachka PW (1980) Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Can J Zool 58:1785–1799
Mommsen TP, Osachoff HL, Elliott ME (2003) Metabolic zonation in teleost gastrointestinal tract. J Comp Physiol B 173:409–418
Montgomery WL, Pollak PE (1988) Gut anatomy and pH in a Red Sea surgeonfish, Acanthurus nigrofuscus. Mar Ecol Prog Ser 44:7–13
Paxton R, Umminger BL (1983) Altered activities of branchial and renal Na/K-and Mg-ATPases in cold-acclimated goldfish (Carassius auratus). Comp Biochem Physiol B 74:503–506
Peres H, Oliva-Teles A (1999) Influence of temperature on protein utilization in juvenile European seabass (Dicentrarchus labrax). Aquaculture 170:337–348
Petersen TD, Hochachka PW, Suarez RK (1987) Hormonal control of gluconeogenesis in rainbow trout hepatocytes: regulatory role of pyruvate kinase. J Exp Zool 243:173–180
Poulsen H, Morth P, Egebjerg J, Nissen P (2010) Phosphorylation of the Na+, K+-ATPase and the H+, K+-ATPase. FEBS Lett 584:2589–2595
Precht H (1958) Concepts of the temperature adaptation of unchanging reaction systems of cold-blooded animals. In: Prosser CL (ed) Physiological adaptations. Am Physiol Soc, Washington DC, pp 50–78
Rubino JG, Zimmer AM, Wood CM (2014) An in vitro analysis of intestinal ammonia handling in fasted and fed freshwater rainbow trout (Oncorhynchus mykiss). J Comp Physiol 184:91–105
Schaarschmidt T, Meyer E, Jürss KA (1999) A comparison of transport-related gill enzyme activities and tissue-specific free amino acid concentrations of Baltic Sea (brackish water) and freshwater threespine sticklebacks, Gasterosteus aculeatus, after salinity and temperature acclimation. Mar Biol 135:689–697
Schnurr ME, Yin Y, Scott GR (2014) Temperature during embryonic development has persistent effects on metabolic enzymes in the muscle of zebrafish. J Exp Biol 217:1370–1380
Shankar RJ, Anderson PM (1985) Purification and properties of glutamate synthetase from liver of Squalus acanthias. Arch Biochem Biophys 239:248–259
Smith MW, Ellory JC (1971) Temperature-induced changes in sodium transport and Na+/K+-adenosine triphosphatase activity in the intestine of goldfish (Carassius auratus L.). Comp Biochem Physiol A 39:209–218
Van Ham EH, Berntssen MH, Imsland AK, Parpoura AC, Bonga SE, Stefansson SO (2003) The influence of temperature and ration on growth, feed conversion, body composition and nutrient retention of juvenile turbot (Scophthalmus maximus). Aquaculture 217:547–558
van den Thillart G, Smit H (1984) Carbohydrate metabolism of goldfish (Carassius auratus L.). J Comp Physiol B 154:477–486
Varis J, Haverinen J, Vornanen M (2016) Lowering temperature is the trigger for glycogen build-up and winter fasting in Crucian Carp (Carassius carassius). Zool Sci 33:83–91
Webb JT, Brown GW (1976) Some properties and occurrence of glutamine synthase in fish. Comp Biochem Physiol 54B:171–175
Webb JT, Brown GWK (1980) Glutamine synthetase: assimilatory role in liver related to urea retention in marine chondrichthyes. Science 208:293–295
Wright PA, Wood CM (2009) A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J Exp Biol 212:2303–2312
Wu B, Luo S, Wang J (2015) Effects of temperature and feeding frequency on ingestion and growth for rare minnow. Physiol Behav 140:197–202
Xu C, Li XF, Tian HY, Jiang GZ, Liu WB (2016) Feeding rates affect growth, intestinal digestive and absorptive capabilities and endocrine functions of juvenile blunt snout bream Megalobrama amblycephala. Fish Physiol Biochem 42:689–700
Yang TH, Somero G (1993) Effects of feeding and food deprivation on oxygen consumption, muscle protein concentration and activities of energy metabolism enzymes in muscle and brain of shallow-living (Scorpaena guttata) and deep-living (Sebastolobus alascanus) scorpaenid fishes. J Exp Biol 181:213–232
Zeng LQ, Li FJ, Li XM, Cao ZD, Fu SJ, Zhang YG (2012) The effects of starvation on digestive tract function and structure in juvenile southern catfish (Silurus meridionalis Chen). Comp Biochem Physiol A 31:200–211
Acknowledgements
CB is supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant and by a Canada Foundation for Innovation John R. Evans Leaders Fund Grant.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I. D. Hume.
Rights and permissions
About this article
Cite this article
Turner, L.A., Bucking, C. The interactive effect of digesting a meal and thermal acclimation on maximal enzyme activities in the gill, kidney, and intestine of goldfish (Carassius auratus). J Comp Physiol B 187, 959–972 (2017). https://doi.org/10.1007/s00360-017-1068-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-017-1068-7