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Dietary plant-protein substitution affects hepatic metabolism in rainbow trout (Oncorhynchus mykiss)

Published online by Cambridge University Press:  09 March 2007

Oddur T. Vilhelmsson ,
Samuel A. M. Martin ,
Françoise Médale ,
Sadasivam J. Kaushik  and
Dominic F. Houlihan
Oddur T. Vilhelmsson*
Affiliation:
School of Biological Sciences, University of Aberdeen, Aberdeen, UK
Samuel A. M. Martin
Affiliation:
School of Biological Sciences, University of Aberdeen, Aberdeen, UK
Françoise Médale
Affiliation:
Fish Nutrition Laboratory, INRA-IFREMER 64310, Saint Pée sur Nivelle, France
Sadasivam J. Kaushik
Affiliation:
Fish Nutrition Laboratory, INRA-IFREMER 64310, Saint Pée sur Nivelle, France
Dominic F. Houlihan
Affiliation:
School of Biological Sciences, University of Aberdeen, Aberdeen, UK
*
*Corresponding author: fax + 44 1224 272396, Email o.vilhelmsson@abdn.ac.uk
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Abstract

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The high dietary protein requirements of salmonid fish are met with fishmeal-based feed in commercial aquaculture. The sustainability of this practice is questionable and, therefore, the feasibility of substituting fishmeal with plant-based products needs to be investigated. We investigated growth and metabolism in rainbow trout (Oncorhynchus mykiss) fed a diet composed of a mixture of plant proteins compared with those fed a fishmeal-based diet. Using two-dimensional gel electrophoresis of liver protein extracts, we showed that the liver protein profile changed in response to the alteration in the diet. A number of metabolic pathways were identified as sensitive to the protein source substitution. These included pathways involved in primary energy generation, maintenance of reducing potential, bile acid synthesis, and transport and cellular protein degradation. Interestingly, the pathways shown to be affected in the present study were somewhat different from those identified in our previous work with soyabean-based-protein replacement of fishmeal, with the effects on the abundance of several stress response proteins notably absent. We conclude, therefore, that the metabolic effects of plant protein replacement in aquaculture feed varies with plant-protein source.

Keywords

ProteomeMass spectrometryTwo-dimensional gel electrophoresisPlant protein
Type
Research Article
Information
British Journal of Nutrition , Volume 92 , Issue 1 , July 2004 , pp. 71 - 80
Copyright
Copyright © The Nutrition Society 2004

References

1Anderson, NL, Esquerblasco, R, Hofmann, JP & Anderson, NGA 2-dimension gel database of rat liver protein useful in gene regulation and drug effect studies. Electrophoresis 1991 12 907–930.CrossRefGoogle Scholar
2Banki, K, Halladay, D & Perl, ACloning and expression of the human gene for transaldolase. J Biol Chem 1994 269, 2847–2851.CrossRefGoogle ScholarPubMed
3Banki, K, Hutter, EColombo, E, Gonchoroff, NJ, Perl, AGlutathione levels and sensitivity to apoptosis are regulated by changes in transaldolase expression. J Biol Chem 1996 271, 32994–33001CrossRefGoogle ScholarPubMed
4Burel, C, Boujard, T, Kaushik, SJ, Boeuf, G, van der Geyten, S, Mol, KA, Kuhn, ER, Quinsac, A, Krouti, M & Ribaillier, DPotential of plant-protein sources as fish meal substitutes in diets for turbot (Psetta maxima): growth, nutrient utilisation and thyroid status. Aquaculture 2000 188, 363–382.CrossRefGoogle Scholar
5Carter, CG & Hauler, RCFish meal replacement by plant meals in extruded feeds for Atlantic salmon, Salmo salar L. Aquaculture 2000 185, 299–311.CrossRefGoogle Scholar
6Cash, P, Argo, E, Ford, L, Lawrie, L & McKenzie, HA proteomic analysis of erythromycin resistance in Streptococcus. Electrophoresis 1999 20, 2259–2268.3.0.CO;2-F>CrossRefGoogle ScholarPubMed
7Cheng, JZ, Hardy, RW & Usry, JLEffects of lysine supplementation in plant protein-based diets on the performance of rainbow trout (Oncorhynchus mykiss) and apparent digestibility coefficients of nutrients. Aquaculture 2003 215, 255–265.CrossRefGoogle Scholar
8Clauser, KR, Baker, PR & Burlingame, ALRole of accurate measurement (+/−10ppm) in protein identification strategies employing MS or MS/MS and database searching. Anal Chem 1999 71, 2871–2882.CrossRefGoogle ScholarPubMed
9Cowey, CBProtein and amino acid requirements: a critique of methods. J Appl Ichthyol 1995 11, 199–204.CrossRefGoogle Scholar
10Cowey, CB & Walton, MJIntermediary metabolism.InFish Nutrition, 2nd ed., 260–329. [Halver, JE, editor]. San Diego, CA Academic Press. 1989Google Scholar
11Davies, SJ & Morris, PCInfluence of multiple amino acid supplementation on the performance of rainbow trout, Oncorhynchus mykiss(Walbaum), fed soya based diets. Aquaculture Res 1997 28, 65–74.CrossRefGoogle Scholar
12Dietrich, A, Dieminger, W, Fuchte, K, Stoll, GH, Schlitz, E, Gerok, W & Kurz, GFunctional significance of interaction of H-FABP with sulfated and nonsulfated taurine-conjugated bile salts in rat liver. J Lipid Res 1995 36, 1745–1755.CrossRefGoogle ScholarPubMed
13Dobly, A, Martin, SAM, Blaney, S & Houlihan, DFEfficiency of conversion of ingested proteins into growth; protein degradation assessed by 20S proteasome activity in rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol 2004 137, 75–85.CrossRefGoogle Scholar
14Eaton, S, Bartlett, K & Pourfarzam, MMammalian mitochondrial β-oxidation. Biochem J 1996 320, 345–357.CrossRefGoogle ScholarPubMed
15Francis, G, Makkar, HPS & Becker, KAntinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 2001 199, 197–227.CrossRefGoogle Scholar
16Gomes, EF, Rema, P, Gouveia, A & Teles, AOReplacement of fish-meal by plant-proteins in diets for rainbow-trout (Oncorhynchus mykiss) – effect of the quality of the fish-meal based control diets on digestibility and nutrient balances. Water Sci Technol 1995 a 31, 205–211.CrossRefGoogle Scholar
17Gomes, EF, Rema, P & Kaushik, SJReplacement of fish-meal by plant-proteins in the diet of rainbow trout (Oncorhynchus mykiss ) – digestibility and growth performance. Aquaculture 1995 b 130, 177–186.CrossRefGoogle Scholar
18Gomez-Requeni, P, Mingarro, M, Kirchner, SEffects of dietary amino acid profile on growth performance, key metabolic enzymes and somatotropic axis responsiveness of gilthead seabream ( Sparus aurata ). Aquaculture 2003 220, 749–767.CrossRefGoogle Scholar
19Hegardt, FGMitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase: a control enzyme in ketogenesis. Biochem J 1999 338, 569–582.CrossRefGoogle ScholarPubMed
20Hogstrand, C, Balesaria, S & Glover, CNApplication of genomics and proteomics for study of the integrated response to zinc exposure in a non-model fish species, the rainbow trout. Comp Biochem Physiol 2002 B 133, 523–535.CrossRefGoogle Scholar
21Jensen, ON, Wilm, M, Shevchenko, A & Mann, MSample preparation methods for mass spectrometric peptide mapping directly from 2-DE gels 2-D Proteome Analysis Protocols, 513–530. [Link, AJ, editor]. New Jersey: Humana Press. 1999Google Scholar
22Kattar-Cooley, PA, Wang, HH, Mende-Mueller, LM & Miziorko, HMAvian liver 3-hydroxy-3-methylglutaryl-CoA synthase: distinct genes encode the cholesterogenic and ketogenic isozymes. Arch Biochem Biophys 1990 283, 523–529.CrossRefGoogle ScholarPubMed
23Kaushik, SJUse of alternative protein sources for the intensive rearing of carnivorous fishes. Mediterranean Aquaculture. pp. 125–138[Flos, R, Tort, L, Torres, P, editors]. ChichesterUK Ellis Horwood 1990Google Scholar
24Kaushik, SJ, Cravedi, JP, Lalles, JP, Sumpter, J, Fauconneau, B & Laroche, MPartial 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 1995 133, 257–274.CrossRefGoogle Scholar
25Krogdahl, A, Lea, TB & Olli, JLSoybean proteinase inhibitors affect intestinal trypsin activities and amino acid digestibilities in rainbow trout (Oncorhynchus mykiss. ). Comp Biochem Physiol A 1994 107, 215–219.CrossRefGoogle Scholar
26Kruger, NJ & von Schaewen, AThe oxidative pentose phosphate pathway: structure and organisation. Curr Opin Plant Biol 2003 6, 236–246.CrossRefGoogle ScholarPubMed
27Lachaise, F, Martin, G, Drougard, C, Perl, A, Vuillaume, M, Wegnez, M, Sarasin, A & Daya-Grosjean, LRelationship between posttranslational modification of transaldolase and catalase deficiency in UV-sensitive repair-deficient xeroderma pigmentosum fibroblasts and SV40-transformed human cells. Free Radic Biol Med 2001 30, 1365–1373.CrossRefGoogle ScholarPubMed
28Mambrini, M, Roem, AJ, Carvedi, JP, Lalles, JP & Kaushik, SJEffects of replacing fish meal with soy protein concentrate and of dl -methionine supplementation in high-energy, extruded diets on the growth and nutrient utilization of rainbow trout, Oncorhynchus mykiss. J Anim Sci 1999 77, 2990–2999.CrossRefGoogle ScholarPubMed
29Martin, SA, Blaney, S, Bowman, AS & Houlihan, DFUbiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss ): effect of food deprivation. Pflugers Arch 2002 445, 257–266.Google ScholarPubMed
30Martin, SAM, Cash, P, Blaney, S & Houlihan, DFProteome analysis of rainbow trout (Oncorhynchus mykiss ) liver proteins during short term starvation. Fish Physiol Biochem 2001 24, 259–270.CrossRefGoogle Scholar
31Martin, SAM, Vilhelmsson, O, Médale, F, Watt, P, Kaushik, S & Houlihan, DFProteomic sensitivity to dietary manipulations in rainbow trout. Biochim Biophys Acta 2003 1651, 17–29.CrossRefGoogle ScholarPubMed
32Médale, F, Boujard, T, Vallée, F, Blanc, D, Mambrini, M, Roem, A & Kaushik, SJVoluntary intake, nitrogen and phosphorus losses in rainbow trout ( Oncorhynchus mykiss ) fed increasing dietary levels of soy protein concentrate. Aquat Living Resour 1998 11, 239–246.CrossRefGoogle Scholar
33Medina, R, Wing, SS & Goldberg, ALIncrease in levels of polyubiquitin and proteasome messenger-RNA in skeletal muscle during starvation and denervation atrophy. Biochem J 1995 307, 631–637.CrossRefGoogle ScholarPubMed
34Moyano, FJ, Gardenete, G & de la Higuera, MNutritive and metabolic utilization of proteins with high glutamic-acid content by the rainbow-trout (Oncorhynchus mykiss). Comp Biochem Physiol A 1991 100, 759–762.CrossRefGoogle Scholar
35Naylor, RL, Goldburg, RJ, Primavera, JH, Kautsky, N, Beveridge, MCM & Clay, JEffect of aquaculture on world fish supplies. Nature 2000 405, 1017–1024.CrossRefGoogle ScholarPubMed
36National Research Council Nutrient Requirements of Fish. Washington, DC: National Academy of Sciences. 1993Google Scholar
37Perkins, DN, Pappin, DJ, Creasy, DM & Cottrell, JSProbability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999 20, 3551–3567.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
38Ricker, WEGrowth rates and models. InBioenergetics and Growth. Fish Physiology,VIII, 677–743 [Hoar, WS, Randall, DJandBrett, JR, editors]. LondonAcademic Press 1979Google Scholar
39Sato, R & Takano, TRegulation of intracellular cholesterol metabolism. Cell Struct Funct 1995 20, 421–427.CrossRefGoogle ScholarPubMed
40Shevchenko, A, Wilm, M, Vorm, O & Mann, MMass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 1996 68, 850–858.CrossRefGoogle ScholarPubMed
41Vielma, J, Makinen, T, Ekholm, P & Koskela, JInfluence of dietary soy and phytase levels on performance and body composition of large rainbow trout ( Oncorhynchus mykiss ) and algal availability of phosphorus load. Aquaculture 2000 183, 349–362.CrossRefGoogle Scholar
42Wilm, M, Shevchenko, A, Houthaeve, T,Breit, S, Schweigerer, L, Fotsis, T & Mann, MFemtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 1996 379, 466–469.CrossRefGoogle ScholarPubMed
43Wilson, RP & Cowey, CBAmino acid composition of whole-body tissue of rainbow trout and Atlantic salmon. Aquaculture 1985 48, 373–376.CrossRefGoogle Scholar
44Wing, SS, Haas, AL & Goldberg, ALIncrease in ubiquitin–protein conjugates concomitant with the increase in proteolysis in rat skeletal muscle during starvation and atrophy denervation. Biochem J 1995 307, 639–645.CrossRefGoogle ScholarPubMed
45Yamamoto, T, Shima, T, Furuita, H & Suzuki, NInfluence of feeding diets with and without fish meal by hand and by self-feeders on feed intake, growth and nutrient utilization of juvenile rainbow trout ( Oncorhynchus mykiss ). Aquaculture 2002 214, 289–305.CrossRefGoogle Scholar