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Relation between growth rate and metabolic organization of white muscle, liver and digestive tract in cod, Gadus morhua

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Abstract

To determine whether the aerobic capacity of tissues required for growth specifically reflects growth rates, we monitored the activities of key enzymes of oxidative, glycolytic and amino acid metabolism in muscle, liver and intestine of Atlantic cod (Gadus morhua) growing at different rates. Fish were maintained individually in small tanks at 10°C and fed on rations that allowed growth rates ranging from-0.6 to 1.6% per day. The correlation between growth rate and muscle enzyme activity was pronounced for the glycolytic enzymes (LDH, PFK and PK). The activities of glycolytic enzymes were more than four times higher for fish having higher growth rates compared to those that did not grow. Mitochondrial enzyme (cytochrome c oxidase, citrate synthase and β-hydroxyacyl-CoA dehydrogenase) activities remained unchanged in fish with positive growth. The liver seems to respond to requirements of growth by an increase in size. In the liver, the activities of the enzymes of amino acid metabolism expressed as units · μg DNA-1 specifically increases with growth rate. In contrast to the two other tissues, the specific activities of mitochondrial enzymes in the intestine increased with growth rate while the relative mass of the intestine remained constant. Intestinal cytochrome c oxidase activity increased from a minimum of about 2 to more than 8 units · g intestine-1. Cytochrome c oxidase activity increased in parallel with the food conversion efficiency. This suggests that the aerobic capacity of the intestine may initially limit the rates of digestion and growth in this species.

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Abbreviations

AA:

amino acid(s)

BM:

body mass

CCO:

cytochrome c oxydase

CS:

citrate synthase

DTNB:

5,5′ dithiobis-2-nitrobenzoic acid

GDH:

glutamate dehydrogenase

GOT:

glutamate oxalacetate transaminase

GPT:

glutamate pyruvate transaminase

GR:

growth rate(s)

HOAD:

β-hydroxyacyl-CoA dehydrogenase

HSI:

hepatosomatic index

LDH:

lactate dehydrogenase

MR:

metabolic rate(s)

PCA:

perchloric acid

PFK:

phosphofructokinase

PK:

pyruvate kinase

PMSF:

phenylmethylsulphonyl fluoride; TRIS

References

  • Baron MG, Adelman IR (1984) Nucleic acid, protein content, and growth of larval fish sublethally exposed to various toxicants. Can J Fish Aquat Sci 41:141–150

    Google Scholar 

  • Beamish FWH (1974) Apparent specific dynamic action of largemouth bass, Micropterus salmoides. J Fish Res Bd Can 31:1763–1769

    Google Scholar 

  • Beamish FWH, Trippel EA (1990) Heat increment: a static or dynamic dimension in bioenergetic models? Trans Am Fish Soc 119:649–661

    Google Scholar 

  • Black D, Love RM (1986) The sequential mobilization and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding. J Comp Physiol B 155:469–479

    Google Scholar 

  • Blaxter K (1989) Energy metabolism in animals and man. Cambridge University Press, Cambridge, U.K.

    Google Scholar 

  • Brawn VM (1961) Aggressive behaviour in the cod (Gadus callarias). Behaviour 18:107–147

    Google Scholar 

  • Brett JR (1976) Feeding metabolic rates of young sockeye salmon, Oncorhynchus nerka, in relation to ration level and temperature. Fish Mar Serv Res Tech Rep 675:43 pp

    Google Scholar 

  • Brown CR, Cameron JN (1991) The relationship between specific dynamic action (SDA) and protein synthesis rates in the channel catfish. Physiol Zool 60:298–309

    Google Scholar 

  • Buchmann K, Borensen T (1988) The effect of different food types and rations on the liver and muscle of cod Gadus morhua. Acta Agric Scand 29:57–59

    Google Scholar 

  • Bulow FJ (1987) RNA-DNA ratios as indicators of growth in fish: a review. In: Summerfelt RC, Hall GE (eds) Age and growth of fish. Iowa State University Press, Ames, pp 45–64

    Google Scholar 

  • Busacker GP, Adelman IR, Goolish EM (1990) Growth. In: Shreck CP, Moyle PP (eds) Methods for fish biology. Academic Press, New York, pp 363–387

    Google Scholar 

  • Clarke ME, Calvi C, Domeirer M, Edmonds M, Walsh PJ (1992) Effects of nutrition and temperature on metabolic enzyme activities in larvae and juvenile red drum, Sciaenops ocellatus, and lanesnapper, Lutjanus synagris. Mar Biol 112:31–36

    Google Scholar 

  • Coulson RA, Hernandez T (1983) Alligator metabolism. Comp Biochem Physiol 74A:59–89

    Google Scholar 

  • Dabrowski KR (1986) A new type of metabolism chamber for the determination of active and postprandial metabolism of fish and consideration of results for coregonid and salmon juveniles. J Fish Biol 28:105–117

    Google Scholar 

  • Dean JC, Donald L, Garling JR, Nielsen LA (1986) Effects of dietary protein quantity and protein quality on growth rate and on selected enzyme activities in channel catfish. Comp Biochem Physiol 83B:355–363

    Google Scholar 

  • Edwards RRC, Finlayson DM, Steele JH (1972) An experimental study of oxygen consumption, growth and metabolism of the cod (Gadus morhua L.). J Exp Mar Biol Ecol 44:299–310

    Google Scholar 

  • Farrell AP, Johansen JA, Suarez RK (1991) Effects of exercise training on cardiac performance and muscle enzymes in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 9:303–312

    Google Scholar 

  • Fauconneau B, Arnal M (1985) In vitro protein synthesis in different tissues and the whole body of rainbow trout (Salmo gairdneri). Influence of environmental temperature. Comp Biochem Physiol 82A:179–187

    Google Scholar 

  • Foster GD, Moon TW (1991) Hypometabolism with fasting in the yellow perch Perca flavescens: a study of enzymes, hepatocyte metabolism, and tissue size. Physiol Zool 64:259–275

    Google Scholar 

  • Goolish EM, Adelman JR (1987) Tissue specific cytochrome oxidase activity in largemouth bass: the metabolic costs of feeding and growth. Physiol Zool 60:454–464

    Google Scholar 

  • Goolish EM, Adelman JR (1988) Tissue specific allometry of an aerobic respiratory enzyme in a large and small species of cyprinid (Teleostei). Can J Zool 66:2199–2208

    Google Scholar 

  • Groen A, Wanders RJA, Westerhoff HS, Van der Meer R, Tagers JM (1982) Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257:2754–2757

    Google Scholar 

  • Hinterleitner S, Huber M, Lackner R, Wieser W (1992) Systemic and enzymatic responses to endurance training in two cyprinid species with different life styles (Teleostei: Cyprinidae). Can J Fish Aquat Sci 49:110–115

    Google Scholar 

  • Hodges TK, Leonard RT (1974) Purification of a plasma membrane bound adenosine triphosphatase from plant roots. In: Fleischer S, Packer L (eds) Methods in enzymology, vol XXXII. Academic Press, New York, pp 392–406

    Google Scholar 

  • Holdway DA, Beamish FWH (1984) Specific growth rate and proximate body composition of Atlantic cod (Gadus morhua L.). J Exp Mar Biol Ecol 81:147–170

    Google Scholar 

  • Houlihan DF, Hall SJ, Gray C (1989) Effect of ration on protein turnover in cod. Aquaculture 79:103–110

    Google Scholar 

  • Houlihan DF, Hall SJ, Gray C, Noble BS (1988) Growth rates and protein turnover in Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 45:951–964

    Google Scholar 

  • Houlihan DF, Laurent P (1987) Effect of exercise training on the performance, growth and protein turnover of rainbow trout Salmo gairdneri. Can J Fish Aquat Sci 44:1614–1621

    Google Scholar 

  • Jobling M (1983) Towards an explanation of specific dynamic action (SDA). J Fish Biol 23:549–555

    Google Scholar 

  • Jobling M (1988) A review of the physiological and nutritional energetics of cod, Gadus morhua L., with particular reference to growth under farmed conditions. Aquaculture 70:1–19

    Google Scholar 

  • Jobling M, Davies PS (1980) Effects of feeding on the metabolic rate and the specific dynamic action in plaice, Pleuronectes platessa L. J Fish Biol 16:629–638

    Google Scholar 

  • Lied E, Rosenlund G, Lund B, Von der Decken A (1983) Effect of starvation and refeeding on in vitro protein synthesis in white trunk muscle of Atlantic cod (Gadus morhua). Comp Biochem Physiol 76B:777–781

    Google Scholar 

  • Loughna PT, Goldspink G (1984) The effects of starvation upon the protein turnover in red and white myotomal muscle of rainbow trout, Salmo gairdneri Richardson. J Fish Biol 25:223–230

    Google Scholar 

  • Mathers EM, Houlihan DF, Cunningham MJ (1992) Nucleic acid concentrations and enzyme activities as correlates of growth rate of the saithe, Pollachius virens: growth-rate estimates of open-sea fish. Mar Biol 112:363–369

    Google Scholar 

  • McMillan DN, Houlihan DF (1989) Short-term responses of protein synthesis to re-feeding in rainbow trout. Aquaculture 79:37–46

    Google Scholar 

  • Miglavs I, Jobling M (1989) Effects of feeding regime of food consumption, growth rates and tissue nucleic acids in juvenile Arctic charr, Salvelinus alpinus, with particular respect to compensatory growth. J Fish Biol 34:947–957

    Google Scholar 

  • Moon TW, Mommsen TP (1987) Enzymes of intermediary metabolism in tissues of the little skate, Raja erinacea. J Exp Zool 244:9–15

    Google Scholar 

  • Munro HN, Fleck A (1966) The determination of nucleic acids. Methods Biochem Anal 14:113–176

    Google Scholar 

  • Pelletier D, Guderley H, Dutil J-D (1993a) Effect of growth rate, temperature and season on glycolytic enzyme activities in white muscle of cod Gadus morhua. J Exp Zool 265:477–487

    Google Scholar 

  • Pelletier D, Guderley H, Dutil J-D (1993b) Does the aerobic capacity of fish muscle change with growth rates? Fish Physiol Biochem 12:83–93

    Google Scholar 

  • Ricker WE (1979) Growth rates and models. In: Haar WS et al. (eds) Fish Physiology, vol 8. Academic Press, New York, pp 677–746

    Google Scholar 

  • Rosenlund G, Lund B, Sanders K, Braekkan OR, Von der Decken A (1984) Muscle protein synthesis in vitro of saithe (Pollachius virens) correlated to growth and daily energy intake. Comp Biochem Physiol 77B:7–13

    Google Scholar 

  • SAS Institute (1985) SAS User's guide: basics and statistics, version 5, edited by SAS Institute. Cary, North Carolina

  • Smith PK, Krohn RI, Hermanson GT, Malia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Google Scholar 

  • Soofiani NM, Hawkins AD (1982) Energetic cost at different levels of feeding in juvenile cod, Gadus morhua. J Fish Biol 21:577–592

    Google Scholar 

  • Sullivan KM, Somero GN (1983) Size-and diet-related variations in enzymic activity and tissue composition in the sablefish, Anaplopoma fimbria. Biol Bull 164:315–326

    Google Scholar 

  • Tager JM, Wanders RJA, Groen AK, Kunz W, Bohnensack R, Kuster U, Letko G, Bohme G, Duszynski J, Wojtczak L (1983) Control of mitochondrial respiration. FEBS Lett 151:1–9

    Google Scholar 

  • Tandler A, Beamish FWH (1981) Apparent specific dynamic action (SDA), fish weight and level of calorie intake in largemouth bass, Micropterus salmoïdes Lacépède. Aquaculture 23:231–242

    Google Scholar 

  • Weatherley AM, Gill HS (1983) Relative growth of tissues at different somatic growth rates in rainbow trout, Salmo gairdneri Richardson. J Fish Biol 22:43–60

    Google Scholar 

  • Weatherley AM, Gill HS (1987) The biology of fish growth. Academic Press, London, pp 147–175

    Google Scholar 

  • Wilson RR (1973) Nitrogen metabolism in channel catfish, Ictalurus punctatus. 1. Tissue distribution of aspartate and alanine aminotransferase and glutamate dehydrogenase. Comp Biochem Physiol 46B:617–624

    Google Scholar 

Download references

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Pelletier, D., Dutil, J.D., Blier, P. et al. Relation between growth rate and metabolic organization of white muscle, liver and digestive tract in cod, Gadus morhua . J Comp Physiol B 164, 179–190 (1994). https://doi.org/10.1007/BF00354078

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