Fish Physiology and Biochemistry

, Volume 42, Issue 2, pp 771–785 | Cite as

Long-term feeding a plant-based diet devoid of marine ingredients strongly affects certain key metabolic enzymes in the rainbow trout liver

  • Vincent Véron
  • Stéphane Panserat
  • Richard Le Boucher
  • Laurent Labbé
  • Edwige Quillet
  • Mathilde Dupont-Nivet
  • Françoise Médale
Article

Abstract

Incorporation of a plant blend in the diet can affect growth parameters and metabolism in carnivorous fish. We studied for the first time the long-term (1 year) metabolic response of rainbow trout fed from first feeding with a plant-based diet totally devoid of marine ingredients. Hepatic enzymes were analyzed at enzymatic and molecular levels, at 3, 8 and 24 h after the last meal to study both the short-term effects of the last meal and long-term effects of the diet. The results were compared with those of fish fed a control diet of fish meal and fish oil. Growth, feed intake, feed efficiency and protein retention were lower in the group fed the plant-based diet. Glucokinase and pyruvate kinase activity were lower in the livers of trout fed the plant-based diet which the proportion of starch was lower than in the control diet. Glutamate dehydrogenase was induced by the plant-based diet, suggesting an imbalance of amino acids and a possible link with the lower protein retention observed. Gene expression of delta 6 desaturase was higher in fish fed the plant-based diet, probably linked to a high dietary level of linolenic acid and the absence of long-chain polyunsaturated fatty acids in vegetable oils. Hydroxymethylglutaryl-CoA synthase expression was also induced by plant-based diet because of the low rate of cholesterol in the diet. Changes in regulation mechanisms already identified through short-term nutritional experiments (<12 weeks) suggest that metabolic responses are implemented at short term and remain in the long term.

Keywords

Fish Nutrition Dietary adaptation Activity Expression 

Abbreviations

M diet

Marine resources-based diet

PB diet

Plant-based diet

GK

Glucokinase

PK

Pyruvate kinase

G6Pase

Glucose 6 phosphatase

GDH

Glutamate dehydrogenase

ASAT

Aspartate aminotransferase

ALAT

Alanine aminotransferase

CS

Citrate synthase

FAS

Fatty acid synthase

HOAD

3-Hydroxyacyl-CoA dehydrogenase

D6D

Delta6desaturase

HMGCS

Hydroxymethylglutaryl-CoA synthase

References

  1. Alami-Durante H, Médale F, Cluzeaud M, Kaushik SJ (2010) Skeletal muscle growth dynamics and expression of related genes in white and red muscles of rainbow trout fed diets with graded levels of a mixture of plant protein sources as substitutes for fishmeal. Aquaculture 303:50–58. doi:10.1016/j.aquaculture.2010.03.012 CrossRefGoogle Scholar
  2. Alegre M, Ciudad CJ, Fillat C, Guinovart JJ (1988) Determination of glucose-6-phosphatase activity using the glucose dehydrogenase-coupled reaction. Anal Biochem 173:185–189. doi:10.1016/0003-2697(88)90176-5 CrossRefPubMedGoogle Scholar
  3. Alvarez MJ, Díez A, López-Bote C et al (2000) Short-term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Br J Nutr 84:619–628PubMedGoogle Scholar
  4. Borrebaek B, Waagbø R, Christophersen B et al (1993) Adaptable hexokinase with low affinity for glucose in the liver of atlantic salmon (Salmo salar). Comp Biochem Physiol Part B Comp Biochem 106:833–836. doi:10.1016/0305-0491(93)90038-7 CrossRefGoogle Scholar
  5. 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
  6. Capilla E, Médale F, Navarro I et al (2003) Muscle insulin binding and plasma levels in relation to liver glucokinase activity, glucose metabolism and dietary carbohydrates in rainbow trout. Regul Pept 110:123–132CrossRefPubMedGoogle Scholar
  7. Chakrabarty K, Leveille GA (1969) Acetyl CoA carboxylase and fatty acid synthetase activities in liver and adipose tissue of meal-fed rats. Exp Biol Med 131:1051–1054CrossRefGoogle Scholar
  8. Chang HC, Seidman I, Teebor G, Lane MD (1967) Liver acetyl CoA carboxylase and fatty acid synthetase: relative activities in the normal state and in hereditary obesity. Biochem Biophys Res Commun 28:682–686CrossRefPubMedGoogle Scholar
  9. Davies SJ, Morris PC, Baker RTM (1997) Partial substitution of fish meal and full-fat soya bean meal with wheat gluten and influence of lysine supplementation in diets for rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Res 28:317–328. doi:10.1046/j.1365-2109.1997.t01-1-00861.x CrossRefGoogle Scholar
  10. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509PubMedGoogle Scholar
  11. Food and Agriculture Organisation (2012) The state of world fisheries and aquaculture. http://www.fao.org/docrep/016/i2727e/i2727e00.htm
  12. Francis G, Makkar HP, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227. doi:10.1016/S0044-8486(01)00526-9 CrossRefGoogle Scholar
  13. Geay F, Ferraresso S, Zambonino-Infante JL et al (2011) Effects of the total replacement of fish-based diet with plant-based diet on the hepatic transcriptome of two European sea bass (Dicentrarchus labrax) half-sibfamilies showing different growth rates with the plant-based diet. BMC Genom 12:522. doi:10.1186/1471-2164-12-522 CrossRefGoogle Scholar
  14. Geurden I, Cuvier A, Gondouin E et al (2005) Rainbow trout can discriminate between feeds with different oil sources. Physiol Behav 85:107–114. doi:10.1016/j.physbeh.2005.03.010 CrossRefPubMedGoogle Scholar
  15. Gómez-Requeni P, Mingarro M, Kirchner S et al (2003) Effects of dietary amino acid profile on growth performance, key metabolic enzymes and somatotropic axis responsiveness of gilthead sea bream (Sparus aurata). Aquaculture 220:749–767. doi:10.1016/S0044-8486(02)00654-3 CrossRefGoogle Scholar
  16. Kaushik SJ, Cravedi JP, Lalles JP et al (1995) Partial or total replacement of fish meal by soybean protein on growth, protein utilization, potential estrogenic or antigenic effects, cholesterolemia and flesh quality in rainbow trout, Oncorhynchus mykiss. Aquaculture 133:257–274. doi:10.1016/0044-8486(94)00403-B CrossRefGoogle Scholar
  17. Kirchner S, Kaushik S, Panserat S (2003) Low protein intake is associated with reduced hepatic gluconeogenic enzyme expression in rainbow trout (Oncorhynchus mykiss). J Nutr 133:2561–2564PubMedGoogle Scholar
  18. Kobayashi A, Jiang LL, Hashimoto T (1996) Two mitochondrial 3-hydroxyacyl-CoA dehydrogenases in bovine liver. J Biochem (Tokyo) 119:775–782CrossRefGoogle Scholar
  19. Kolditz C, Borthaire M, Richard N et al (2008) Liver and muscle metabolic changes induced by dietary energy content and genetic selection in rainbow trout (Oncorhynchus mykiss). AJP Regul Integr Comp Physiol 294:R1154–R1164. doi:10.1152/ajpregu.00766.2007 CrossRefGoogle Scholar
  20. Krogdahl Å, Lea TB, Olli JJ (1994) Soybean proteinase inhibitors affect intestinal trypsin activities and amino acid digestibilities in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A Physiol 107:215–219. doi:10.1016/0300-9629(94)90296-8 CrossRefGoogle Scholar
  21. Le Boucher R, Quillet E, Vandeputte M et al (2011) Plant-based diet in rainbow trout (Oncorhynchus mykiss Walbaum): are there genotype-diet interactions for main production traits when fish are fed marine versus plant-based diets from the first meal? Aquaculture 321(1–2):41–48. doi:10.1016/j.aquaculture.2011.08.010 CrossRefGoogle Scholar
  22. Le Boucher R, Dupont-Nivet M, Vandeputte M et al (2012a) Selection for adaptation to dietary shifts: towards sustainable breeding of carnivorous fish. PLoS ONE 7:e44898. doi:10.1371/journal.pone.0044898 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Le Boucher R, Vandeputte M, Dupont-Nivet M et al (2012b) Genotype by diet interactions in European sea bass (Dicentrarchus labrax L.): nutritional challenge with totally plant-based diets. J Anim Sci 91:44–56. doi:10.2527/jas.2012-5311 CrossRefPubMedGoogle Scholar
  24. Lund I, Dalsgaard J, Rasmussen HT et al (2011) Replacement of fish meal with a matrix of organic plant proteins in organic trout (Oncorhynchus mykiss) feed, and the effects on nutrient utilization and fish performance. Aquaculture 321:259–266. doi:10.1016/j.aquaculture.2011.09.028 CrossRefGoogle Scholar
  25. Martin SAM, Vilhelmsson O, Médale F et al (2003) Proteomic sensitivity to dietary manipulations in rainbow trout. Biochim Biophys Acta BBA Proteins Proteomics 1651:17–29. doi:10.1016/S1570-9639(03)00231-0 CrossRefPubMedGoogle Scholar
  26. 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 B: Biochem Mol Biol 138:145–153. doi:10.1016/j.cbpc.2004.03.004 CrossRefGoogle Scholar
  27. Montero D, Mathlouthi F, Tort L et al (2010) Replacement of dietary fish oil by vegetable oils affects humoral immunity and expression of pro-inflammatory cytokines genes in gilthead sea bream Sparus aurata. Fish Shellfish Immunol 29:1073–1081. doi:10.1016/j.fsi.2010.08.024 CrossRefPubMedGoogle Scholar
  28. Moon TW (2001) Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B: Biochem Mol Biol 129:243–249CrossRefGoogle Scholar
  29. Moyano F, Cardenete G, De la Higuera M (1991) Nutritive and metabolic utilization of proteins with high glutamic acid content by the rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A Physiol 100:759–762. doi:10.1016/0300-9629(91)90404-Z CrossRefGoogle Scholar
  30. National Research Council (U. S.) (2011) Nutrient requirements of fish and shrimp. National Academies Press, WashingtonGoogle Scholar
  31. Panserat S, Médale F, Blin C et al (2000a) Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilthead seabream, and common carp. Am J Physiol Regul Integr Comp Physiol 278:R1164–R1170PubMedGoogle Scholar
  32. Panserat S, Médale F, Brèque J et al (2000b) Lack of significant long-term effect of dietary carbohydrates on hepatic glucose-6-phosphatase expression in rainbow trout (Oncorhynchus mykiss). J Nutr Biochem 11:22–29CrossRefPubMedGoogle Scholar
  33. Panserat S, Plagnes-Juan E, Kaushik S (2001) Nutritional regulation and tissue specificity of gene expression for proteins involved in hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204:2351–2360PubMedGoogle Scholar
  34. Panserat S, Kolditz C, Richard N et al (2008) Hepatic gene expression profiles in juvenile rainbow trout (Oncorhynchus mykiss) fed fishmeal or fish oil-free diets. Br J Nutr 100:953. doi:10.1017/S0007114508981411 CrossRefPubMedGoogle Scholar
  35. Panserat S, Hortopan GA, Plagnes-Juan E et al (2009) Differential gene expression after total replacement of dietary fish meal and fish oil by plant products in rainbow trout (Oncorhynchus mykiss) liver. Aquaculture 294:123–131. doi:10.1016/j.aquaculture.2009.05.013 CrossRefGoogle Scholar
  36. Pérez-Jiménez A, Cardenete G, Hidalgo MC et al (2012) Metabolic adjustments of Dentex dentex to prolonged starvation and refeeding. Fish Physiol Biochem 38:1145–1157. doi:10.1007/s10695-011-9600-2 CrossRefPubMedGoogle Scholar
  37. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45CrossRefPubMedPubMedCentralGoogle Scholar
  38. Pilkis SJ, Granner DK (1992) Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annu Rev Physiol 54:885–909. doi:10.1146/annurev.ph.54.030192.004321 CrossRefPubMedGoogle Scholar
  39. Polakof S, Panserat S, Soengas JL, Moon TW (2012) Glucose metabolism in fish: a review. J Comp Physiol 182:1015–1045. doi:10.1007/s00360-012-0658-7 CrossRefGoogle Scholar
  40. Řehulka J, Minařík B (2012) Cholesterolaemia and triacylglycerolaemia in farmed rainbow trout, Oncorhynchus mykiss. Aquac Res 43:1651–1659. doi:10.1111/j.1365-2109.2011.02971.x CrossRefGoogle Scholar
  41. Richard N, Kaushik S, Larroquet L et al (2007) Replacing dietary fish oil by vegetable oils has little effect on lipogenesis, lipid transport and tissue lipid uptake in rainbow trout (Oncorhynchus mykiss). Br J Nutr 96:299. doi:10.1079/BJN20061821 CrossRefGoogle Scholar
  42. Seiliez I, Panserat S, Kaushik S, Bergot P (2001) Cloning, tissue distribution and nutritional regulation of a Δ6-desaturase-like enzyme in rainbow trout. Comp Biochem Physiol B: Biochem Mol Biol 130:83–93. doi:10.1016/S1096-4959(01)00410-9 CrossRefGoogle Scholar
  43. Singer TD, Mahadevappa VG, Ballantyne JS (1990) Aspects of the energy metabolism of lake sturgeon, Acipenser fulvescens, with special emphasis on lipid and ketone body metabolism. Can J Fish Aquat Sci 47:873–881. doi:10.1139/f90-100 CrossRefGoogle Scholar
  44. Slawski H, Adem H, Tressel R-P et al (2011) Total fish meal replacement with rapeseed protein concentrate in diets fed to rainbow trout (Oncorhynchus mykiss Walbaum). Aquac Int 20:443–453. doi:10.1007/s10499-011-9476-2 CrossRefGoogle Scholar
  45. Soengas JL, Polakof S, Chen X et al (2006) Glucokinase and hexokinase expression and activities in rainbow trout tissues: changes with food deprivation and refeeding. Am J Physiol Regul Integr Comp Physiol 291:R810–R821. doi:10.1152/ajpregu.00115.2006 CrossRefPubMedGoogle Scholar
  46. Stickney RR, Hardy RW, Koch K et al (1996) The effects of substituting selected oilseed protein concentrates for fish meal in rainbow trout Oncorhynchus mykiss diets. J World Aquac Soc 27:57–63. doi:10.1111/j.1749-7345.1996.tb00594.x CrossRefGoogle Scholar
  47. Tacchi L, Secombes CJ, Bickerdike R et al (2012) Transcriptomic and physiological responses to fishmeal substitution with plant proteins in formulated feed in farmed Atlantic salmon (Salmo salar). BMC Genom 13:363. doi:10.1186/1471-2164-13-363 CrossRefGoogle Scholar
  48. Thanuthong T, Francis DS, Manickam E et al (2011a) Fish oil replacement in rainbow trout diets and total dietary PUFA content: II Effects on fatty acid metabolism and in vivo fatty acid bioconversion. Aquaculture 322–323:99–108. doi:10.1016/j.aquaculture.2011.09.026 CrossRefGoogle Scholar
  49. Thanuthong T, Francis DS, Senadheera SD et al (2011b) Fish oil replacement in rainbow trout diets and total dietary PUFA content: I Effects on feed efficiency, fat deposition and the efficiency of a finishing strategy. Aquaculture 320:82–90. doi:10.1016/j.aquaculture.2011.08.007 CrossRefGoogle Scholar
  50. The R Project for Statistical Computing (2013) http://www.r-project.org/. Accessed 3 Dec 2013
  51. Torstensen BE, Espe M, Sanden M et al (2008) Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture 285:193–200. doi:10.1016/j.aquaculture.2008.08.025 CrossRefGoogle Scholar
  52. Turchini GM, Francis DS (2009) Fatty acid metabolism (desaturation, elongation and β-oxidation) in rainbow trout fed fish oil- or linseed oil-based diets. Br J Nutr 102:69. doi:10.1017/S0007114508137874 CrossRefPubMedGoogle Scholar
  53. Vagner M, Santigosa E (2011) Characterization and modulation of gene expression and enzymatic activity of delta-6 desaturase in teleosts: a review. Aquaculture 315:131–143. doi:10.1016/j.aquaculture.2010.11.031 CrossRefGoogle Scholar
  54. Vilhelmsson OT, Martin SAM, Médale F et al (2004) Dietary plant-protein substitution affects hepatic metabolism in rainbow trout (Oncorhynchus mykiss). Br J Nutr 92:71. doi:10.1079/BJN20041176 CrossRefPubMedGoogle Scholar
  55. Zhang Y, Øverland M, Shearer KD et al (2012) Optimizing plant protein combinations in fish meal-free diets for rainbow trout (Oncorhynchus mykiss) by a mixture model. Aquaculture 360–361:25–36. doi:10.1016/j.aquaculture.2012.07.003 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Vincent Véron
    • 1
  • Stéphane Panserat
    • 1
  • Richard Le Boucher
    • 2
  • Laurent Labbé
    • 3
  • Edwige Quillet
    • 2
  • Mathilde Dupont-Nivet
    • 2
  • Françoise Médale
    • 1
  1. 1.INRA UR 1067 NuMeA (Nutrition Metabolism Aquaculture)Saint Pée Sur NivelleFrance
  2. 2.INRA, UMR1313 GABI (Génétique animale et biologie intégrative)Jouy-En-JosasFrance
  3. 3.INRA, UE 0937 PEIMA (Pisciculture Expérimentale INRA des Monts d’Arrée)SizunFrance

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