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Dietary fatty acid composition changes mitochondrial phospholipids and oxidative capacities in rainbow trout red muscle

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Abstract

Dietary conditioning of juvenile trout changed the acyl chain composition of mitochondrial phospholipids and the oxidative capacities of muscle mitochondria. Trout were fed three diets differing only in fatty acid (FA) composition. The highly unsaturated 22:6 n-3 (DHA) accounted for 0.4, 14, and 30% of fatty acids in Diets 1, 2 and 3. After 10 weeks of growth, the dietary groups differed markedly in FA composition of mitochondrial phospholipids, with significant dietary effects for virtually all FA. Mean mitochondrial DHA levels were 19, 40 and 33% in trout fed Diets 1, 2 and 3. Mitochondrial oxidative capacities changed with diet, while mitochondrial concentrations of cytochromes and of the adenylate nucleotide translocase (nmol mg1 protein) did not. Mitochondria from fish fed Diet 1 had higher non-phosphorylating (state 4) rates at 5°C than those fed other diets. When phosphorylating (state 3) rates differed between dietary groups, rates at 5 and 15°C were higher for fish fed the more unsaturated diets. Stepwise multiple regressions indicated that FA composition could explain much (42–70%) of the variability of state 4 rates, particularly at 5°C. At 15°C, FA composition explained 16–42% of the variability of states 3 and 4 rates. Similar conclusions were obtained for the complete data set (trout fed diets 1, 2 and 3) and for the data from trout achieving similar growth rates (e.g. those fed Diets 1 and 2). Neither general characteristics of membrane FA, such as % saturates, unsaturation index, n-3, n-6 or n-3/n-6 nor levels of abundant unsaturated FA such as DHA or 18:1(n-9 + n-7), were systematically correlated with mitochondrial capacities even though they differed considerably between trout fed the different diets. Relatively minor FA (20:5n-3, 20:0, 18:2n-6, 18:3n-3, 18:0 and 15:0) showed better correlations with mitochondrial oxidative capacities. This supports the concept that acyl chain composition modulates mitochondrial capacities via interactions between membrane proteins and specific FA of particular phospholipid classes in their microenvironment.

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References

  • Berger A, German JB, Gershwin ME (1993) Biochemistry of CL: sensitivity to dietary fatty acids. In: Kissela JE (ed) Advances in food and nutrition research, vol 37. Academic Press, San Diego, pp 259–338

  • Bernard SF, Reidy SP, Zwingelstein G, Weber J-M (1999) Glycerol and fatty acid kinetics in rainbow trout: effects of endurance swimming. J Exp Biol 202:279–288

    PubMed  CAS  Google Scholar 

  • Blier PU, Lemieux H (2001) The impact of the thermal sensitivity of cytochrome C oxidase on the respiration rate of Arctic charr red muscle mitochondria. J Comp Physiol 171:246–253

    Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    PubMed  CAS  Google Scholar 

  • Bouchard P, Guderley H (2003) Time course of the response of mitochondria from oxidative muscle during thermal acclimation of rainbow trout, Oncorhynchus mykiss. J Exp Biol 206:3455–3465

    Article  PubMed  CAS  Google Scholar 

  • Brand MD, Turner N, Ocloo A, Else PL, Hulbert AJ (2003) Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds. Biochem J 376:741–748

    Article  PubMed  CAS  Google Scholar 

  • Brookes PS, Buckingham JA, Tenreiro AM, Hulbert AJ, Brand MD (1998) The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp Biochem Physiol 119B:325–334

    CAS  Google Scholar 

  • Canadian Council on Animal Care (1984) Guide to the care and use of experimental animals, vol 2. Canadian Council on Animal Care, Ottowa

    Google Scholar 

  • Carey C, Hazel JR (1989) Diurnal variation in membrane lipid composition of Sonoran desert teleosts. J Exp Biol 147:375–391

    CAS  Google Scholar 

  • Cho CY (1992) Feeding systems for rainbow trout and other salmonids with reference to current estimates of energy and protein requirements. Aquaculture 100:107–123

    Article  Google Scholar 

  • Clandinin MT, Field CJ, Hargraves K, Morson L, Zsigmond E (1985) Role of diet fat in subcellular structure and function. Can J Physiol Pharm 63:546–556

    CAS  Google Scholar 

  • Cuculescu M, Pearson T, Hyde D, Bowler K (1999) Heterothermal acclimation: an experimental paradigm for studying the control of thermal acclimation in crabs. Proc Natl Acad Sci USA 96:6501–6505

    Article  PubMed  CAS  Google Scholar 

  • Daum G (1985) Lipids of mitochondria. Biochim Biophys Acta 822:1–42

    PubMed  CAS  Google Scholar 

  • Divakaran P,Venkataram A (1977) Effect of dietary fats on oxidative phosphorylation and fatty acid profile of rat liver mitochondria. J Nutr 107:1621–1631

    PubMed  CAS  Google Scholar 

  • Egginton S (1996) Effect of temperature on optimal substrate for β-oxidation. J Fish Biol 49:753–758

    CAS  Google Scholar 

  • Forman NG, Wilson DF (1983) Dependence of mitochondrial oxidative phosphorylation on activity of the adenine nucleotide translocase. J Biol Chem 258:8649–8655

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Guderley H, St-Pierre J, Couture P, Hulbert AJ (1997) Plasticity of the properties of mitochondria from rainbow trout red muscle with seasonal acclimatization. Fish Physiol Biochem 16:531–541

    Article  CAS  Google Scholar 

  • Guderley H, Turner N, Else PL, Hulbert AJ (2005) Why are some mitochondria more powerful than others: insights from comparisons of muscle mitochondria from three terrestrial vertebrates. Comp Biochem Physiol Part B 142:172–180

    Article  Google Scholar 

  • Hazel JR (1972a) 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:837–861

    Google Scholar 

  • Hazel JR (1972b) The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus L.)—II. Lipid reactivation of the soluble enzyme. Comp Biochem Physiol 43B:863–882

    Google Scholar 

  • Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42

    PubMed  CAS  Google Scholar 

  • Hazel JR, Landrey SR (1988a) Time course of thermal adaptation in plasma membranes of trout kidney I. Headgroup composition. Am J Physiol 255:R622–R627

    PubMed  CAS  Google Scholar 

  • Hazel JR, Landrey SR (1988b) Time course of thermal adaptation in plasma membranes of trout kidney II. Molecular species composition. Am J Physiol 255:R628–R634

    PubMed  CAS  Google Scholar 

  • Henderson RJ, Tocher DR (1987) Lipid composition and biochemistry of freshwater ?sh. Prog Lipid Res 26:281–347

    Article  PubMed  CAS  Google Scholar 

  • Hoch FL (1992) Cardiolipins and biomembrane function. Biochim Biophys Acta 1113:71–133

    PubMed  CAS  Google Scholar 

  • Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of metabolism. J Theor Biol 199:257–274

    Article  PubMed  CAS  Google Scholar 

  • Hulbert AJ, Else PL (2000) Mechanisms underlying the cost of living in animals. Annu Rev Physiol 62:207–235

    Article  PubMed  CAS  Google Scholar 

  • Hulbert AJ, Faulks S, Buttemer WA, Else PL (2002) Acyl composition of muscle membranes varies with body size in birds. J Exp Biol 205:3561–3569

    PubMed  CAS  Google Scholar 

  • Hulbert AJ, Turner N, Storlein LH, Else PL (2005) Dietary fats and membrane function: implications for metabolism and disease. Biol Rev 80:155–169

    Article  PubMed  CAS  Google Scholar 

  • Hulbert AJ, Turner N, Hinde J, Else PL, Guderley H (2006) How might you compare mitochondria from different tissues and different species? J Comp Physiol B 176:93–105

    Article  PubMed  CAS  Google Scholar 

  • Kraffe E, Marty Y, Guderley H (2007) Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins, phospholipids and their fatty acid compositions. J Exp Biol 210:149–165

    Article  PubMed  CAS  Google Scholar 

  • Krämer R, Klingenberg M (1980) Enhancement of reconstituted ADP, ATP exchange activity by phosphatidylethanolamine and by anionic phospholipids. FEBS Lett 119:257–261

    Article  PubMed  Google Scholar 

  • Liu S, Baracos VE, Quinney A, Clandinin MT (1994) Dietary ω-3 and polyunsaturated fatty acids modify fatty acyl composition and insulin binding in skeletal-muscle sarcolemma. Biochem J 299:831–837

    PubMed  CAS  Google Scholar 

  • McKenzie DJ, Higgs DA, Dosanjh BS, Deacon G, Randall DJ (1998) Dietary fatty acid composition influences swimming performance in Atlantic salmon (Salmo salar) in seawater. Fish Physiol Biochem 19:111–122

    Article  CAS  Google Scholar 

  • Miranda EJ, Hazel JR (1996) Temperature-induced changes in the transbilayer distribution of phosphatidylethanolamine in mitoplasts of rainbow trout (Oncorhynchus mykiss) liver. J Exp Zool 274:23–32

    Article  CAS  Google Scholar 

  • Miranda EJ, Hazel JR (2002) The effect of acclimation temperature on the fusion kinetics of lipid vesicles derived from endoplasmic reticulum membranes of rainbow trout (Oncorhynchus mykiss) liver. Comp Biochem Physiol Part A 131:275–286

    Article  Google Scholar 

  • National Research Council (NRC) (1993) Nutrient requirements of fish. National Academy Press, Washington DC

    Google Scholar 

  • Paradies G, Petrosillo G, Pistolese M, Ruggiere FM (2002) Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 286:135–141

    Article  PubMed  CAS  Google Scholar 

  • Pearson T, Hyde D, Bowler K (1999) Heterologous acclimation: a novel approach to the study of thermal acclimation in the crab Cancer pagurus. Am J Physiol 277:R24–R30

    PubMed  CAS  Google Scholar 

  • Porter RK, Hulbert AJ, Brand MD (1996) Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am J Physiol 271:R1550–R1556

    PubMed  CAS  Google Scholar 

  • Renner R, Innis SM, Clandinin MT (1979) Effects of high and low erucic acid rapeseed oils on energy metabolism and mitochondrial function of the chick. J Nutr 109:378–387

    PubMed  CAS  Google Scholar 

  • Rolfe DFS, Brand MD (1996) Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am J Physiol 271:C1380–C1389

    PubMed  CAS  Google Scholar 

  • Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    PubMed  CAS  Google Scholar 

  • Rolfe DFS, Newman JMB, Buckingham JA, Clark MG, Brand MD (1999) Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol 276:C692–C699

    PubMed  CAS  Google Scholar 

  • Rollin X, Peng J, Pham D, Ackman RG, Larondelle Y (2003) The effects of dietary lipid and strain difference on polyunsaturated fatty acid composition and conversion in anadromous and landlocked salmon (Salmo salar L.) parr. Comp Biochem Physiol 134B:349–366

    CAS  Google Scholar 

  • Sargent JR, Bell G, McEvoy LA, Tocher D, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199

    Article  CAS  Google Scholar 

  • Sargent JR, Tocher DR, Bell JG (2002) The lipids. In: Halver JE, Hard RW (eds) Fish nutrition. Academic Press, London, pp 182–257

    Google Scholar 

  • SAS Institute (1988) SAS/STAT user’s guide, release 6.03 ed. SAS Institute, Cary

    Google Scholar 

  • Schlame M, Rua D, Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39:257–288

    Article  PubMed  CAS  Google Scholar 

  • Schneider H, Lemasters JJ, Höchli M, Hackenbrock CR (1980) Liposome-mitochondrial inner membrane fusion. J Biol Chem 255:3748–3756

    PubMed  CAS  Google Scholar 

  • Sidell BD, Crockett EL, Driedzic WR (1995) Antarctic fish tissues preferentially catabolize monenoic fatty acids. J Exp Zool 271:73–81

    Article  CAS  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia 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

    Article  PubMed  CAS  Google Scholar 

  • Steffens W (1997) Effects of variation in essential fatty acids in fish feeds on nutritive value of freshwater fish for humans. Aquaculture 151:97–119

    Article  CAS  Google Scholar 

  • St-Pierre J, Charest PM, Guderley H (1998) Relative contribution of quantitative and qualitative changes in mitochondria to metabolic compensation during seasonal acclimatisation of rainbow trout, Oncorhynchus mykiss. J Exp Biol 201:2961–2970

    CAS  Google Scholar 

  • Wagner GN, Balfry SK, Higgs DA, Lull SP, Farrell AP (2004) Dietary fatty acid composition affects the repeat swimming performance of Atlantic salmon in seawater. Comp Biochem Physiol 137A:567–576

    CAS  Google Scholar 

  • Weber J-M, Brichon G, Bodennec J, Zwingelstein G (2002) Palmitate and oleate metabolism of rainbow trout in vivo. Comp Biochem Physiol 131A:409–416

    CAS  Google Scholar 

  • Williams Jr JN (1964) A method for the simultaneous quantitative estimation of cytochromes A, B, C1 and C in mitochondria. Arch Biochem Biophys 107:537–543

    Article  PubMed  CAS  Google Scholar 

  • Willis WT, Dallman PR (1983) Impaired control of respiration in iron deficient mitochondria. Am J Physiol 257:C1080–C1085

    Google Scholar 

  • Wu BJ, Else PL, Storlein LH, Hulbert AJ (2001) Molecular activity of Na+/K+ ATPase from different sources is related to the packing of membrane lipids. J Exp Biol 204:4271–4280

    PubMed  CAS  Google Scholar 

  • Yamaoka S, Urade R, Kito M (1988) Mitochondrial function in rats is affected by modification of membrane phospholipids with dietary sardine oil. J Nutr 118:290–96

    PubMed  CAS  Google Scholar 

  • Yamaoka S, Urade R, Kito M (1990) Cardiolipin molecular species in rat heart mitochondria are sensitive to essential fatty acid-deficient dietary lipids. J Nutr 120:415–421

    PubMed  CAS  Google Scholar 

  • Yamakaoka-Koseki S, Urade R, Kito M (1991) Cardiolipins from rats fed different dietary lipids affect bovine heart cytochrome c oxidase activity. J Nutr 121:956–958

    Google Scholar 

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Acknowledgments

Marika Deschambeault and Julie Labrie provided excellent technical assistance during the respirometry studies. The authors extend their sincere thanks to Matthew Bancroft for care of the experimental animals during the growth trial. This research was supported by Discovery grants from NSERC to HG and DPB. EK received partial salary support from the Reseau Aquacole du Québec.

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Authors and Affiliations

  1. Département de Biologie, Université Laval, G1K 7P4, Quebec, QC, Canada

    H. Guderley & E. Kraffe

  2. UG/OMNR Fish Nutrition Research Laboratory, Department of Animal and Poultry Science, University of Guelph, N1G 2W1, Guelph, ON, Canada

    W. Bureau & D. P. Bureau

  3. Unité mixte CNRS 6521, Université de Bretagne Occidentale, C.S. 93837, 29238, Brest cedex 3, France

    E. Kraffe

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  1. H. Guderley
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Correspondence to H. Guderley.

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Communicated by H.V. Carey.

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Guderley, H., Kraffe, E., Bureau, W. et al. Dietary fatty acid composition changes mitochondrial phospholipids and oxidative capacities in rainbow trout red muscle. J Comp Physiol B 178, 385–399 (2008). https://doi.org/10.1007/s00360-007-0231-y

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  • DOI: https://doi.org/10.1007/s00360-007-0231-y

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