Fish Physiology and Biochemistry

, Volume 42, Issue 4, pp 1187–1202 | Cite as

Postprandial kinetics of gene expression of proteins involved in the digestive process in rainbow trout (O. mykiss) and impact of diet composition

  • Marion Borey
  • Stephane Panserat
  • Anne Surget
  • Marianne Cluzeaud
  • Elisabeth Plagnes-Juan
  • Alexandre Herman
  • Viviana Lazzarotto
  • Geneviève Corraze
  • Françoise Médale
  • Beatrice Lauga
  • Christine Burel
Article

Abstract

The impact of increased incorporation of plant ingredients on diets for rainbow trout was evaluated in terms of gene expression of gastric (gastric lipase, pepsinogen) and intestinal (prolidase, maltase, phospholipase A2) digestive enzymes and nutrient transporters (peptide and glucose transporters), as well as of postprandial levels of plasma glucose, triglycerides and total free amino acids. For that purpose, trout alevins were fed from the start of exogenous feeding one of three different experimental diets: a diet rich in fish meal and fish oil (FM–FO), a plant-based diet (noFM–noFO) totally free from fish meal and fish oil, but containing plant ingredients and a Mixed diet (Mixed) intermediate between the FM–FO and noFM–noFO diets. After 16 months of rearing, all fish were left unfed for 72 h and then given a single meal to satiation. Blood, stomach and anterior intestine were sampled before the meal and at 2, 6 and 12 h after this meal. The postprandial kinetics of gene expression of gastric and intestinal digestive enzymes and nutrient transporters were then followed in trout fed the FM–FO diet. The postprandial profiles showed that the expression of almost all genes studied was stimulated by the presence of nutrients in the digestive tract of trout, but the timing (appearance of peaks) varied between genes. Based on these data, we have focused on the molecular response to dietary factors in the stomach and the intestine at 6 and 12 h after feeding, respectively. The reduction in FM and FO levels of dietary incorporation induced a significant decrease in the gene expression of gastric lipase, GLUT2 and PEPT1. The plasma glucose and triglycerides levels were also reduced in trout fed the noFM–noFO diet. Consequently, the present study suggests a decrease in digestive capacities in trout fed a diet rich in plant ingredients.

Keywords

Rainbow trout Plant-based diet Nutrient transporters Digestive enzymes 

References

  1. Azarm HM, Kenari AA, Hedayati M (2013) Effect of dietary phospholipid sources and levels on growth performance, Enzymes activity, Cholecystokinin and lipoprotein fractions of rainbow trout (Oncorhynchus mykiss) fry. Aquac Res 44:634–644. doi:10.1111/j.1365-2109.2011.03068.x CrossRefGoogle Scholar
  2. Azodi M, Ebrahimi E, Motaghi E, Morshedi V (2015) Metabolic responses to short starvation and re-feeding in rainbow trout (Oncorhynchus mykiss). Ichthyol Res 62:177–183. doi:10.1007/s10228-014-0421-z CrossRefGoogle Scholar
  3. Basque JR, Ménard D (2000) Establishment of culture systems of human gastric epithelium for the study of pepsinogen and gastric lipase synthesis and secretion. Microsc Res Tech 48:293–302. doi:10.1002/(SICI)1097-0029(20000301)48:5<293:AID-JEMT6>3.0.CO;2-A CrossRefPubMedGoogle Scholar
  4. Borovicka J, Schwizer W, Guttmann G et al (2000) Role of lipase in the regulation of postprandial gastric acid secretion and emptying of fat in humans: a study with orlistat, a highly specific lipase inhibitor. Gut 46:774–781. doi:10.1136/gut.46.6.774 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bucking C, Wood CM (2006) Water dynamics in the digestive tract of the freshwater rainbow trout during the processing of a single meal. J Exp Biol 209:1883–1893. doi:10.1242/jeb.02205 CrossRefPubMedGoogle Scholar
  6. Caballero M, Obach A, Rosenlund G et al (2002) Impact of different dietary lipid sources on growth, lipid digestibility, tissue fatty acid composition and histology of rainbow trout, Oncorhynchus mykiss. Aquaculture 214:253–271. doi:10.1016/S0044-8486(01)00852-3 CrossRefGoogle Scholar
  7. Castro C, Couto A, Pérez-Jiménez A et al (2016) Effects of fish oil replacement by vegetable oil blend on digestive enzymes and tissue histomorphology of European sea bass (Dicentrarchus labrax) juveniles. Fish Physiol Biochem 42(1):203–217. doi:10.1007/s10695-015-0130-1 CrossRefPubMedGoogle Scholar
  8. Coutteau P, Geurden I, Camara MR et al (1997) Review on the dietary effects of phospholipids in fish and crustacean larviculture. Aquaculture 155:149–164. doi:10.1016/S0044-8486(97)00125-7 CrossRefGoogle Scholar
  9. Dabrowski K, Dabrowska H (1981) Digestion of protein by rainbow trout (Salmo gairdneri Rich.) and absorption of amino acids within the alimentary tract. Comp Biochem Physiol Part A Physiol 69:99–111. doi:10.1016/0300-9629(81)90643-5 CrossRefGoogle Scholar
  10. Fauconneau B, Choubert G, Blanc D et al (1983) Influence of environmental temperature on flow rate of foodstuffs through the gastrointestinal tract of rainbow trout. Aquaculture 34:27–39CrossRefGoogle Scholar
  11. Ferraris RP, Ahearn G (1984) Sugar and amino acid transport in fish intestine. Comp Biochem Physiol Part A Physiol 77:397–413. doi:10.1016/0300-9629(84)90204-4 CrossRefGoogle Scholar
  12. Geurden I, Aramendi M, Zambonino-Infante JL, Panserat S (2007) Early feeding of carnivorous rainbow trout (Oncorhynchus mykiss) with a hyperglucidic diet during a short period: effect on dietary glucose utilization in juveniles. Am J Physiol Regul Integr Comp Physiol 292:R2275–R2283. doi:10.1152/ajpregu.00444.2006 CrossRefPubMedGoogle Scholar
  13. Geurden I, Borchert P, Balasubramanian MN et al (2013) The positive impact of the early-feeding of a plant-based diet on its future acceptance and utilisation in rainbow trout. PLoS ONE. doi:10.1371/journal.pone.0083162 Google Scholar
  14. Geurden I, Mennigen J, Plagnes-Juan E et al (2014) High or low dietary carbohydrate:protein ratios during first-feeding affect glucose metabolism and intestinal microbiota in juvenile rainbow trout. J Exp Biol 217(19):3396–3406CrossRefPubMedGoogle Scholar
  15. Glencross B, Evans D, Rutherford N et al (2006) The influence of the dietary inclusion of the alkaloid gramine, on rainbow trout (Oncorhynchus mykiss) growth, feed utilisation and gastrointestinal histology. Aquaculture 253:512–522. doi:10.1016/j.aquaculture.2005.07.009 CrossRefGoogle Scholar
  16. Gómez-Requeni P, Calduch-Giner J, Vega-Rubín de Celis S et al (2005) Regulation of the somatotropic axis by dietary factors in rainbow trout (Oncorhynchus mykiss). Br J Nutr 94:353–361. doi:10.1079/BJN20051521 CrossRefPubMedGoogle Scholar
  17. Heckmann L-H, Sørensen PB, Krogh PH, Sørensen JG (2011) NORMA-Gene: a simple and robust method for qPCR normalization based on target gene data. BMC Bioinf 12:250–257. http://www.biomedcentral.com/1471-2105/12/250
  18. Hua K, Bureau D (2012) Exploring the possibility of quantifying the effects of plant protein ingredients in fish feeds using meta-analysis and nutritional model simulation-based approaches. Aquaculture 356–357:284–301. doi:10.1016/j.aquaculture.2012.05.003 CrossRefGoogle Scholar
  19. Ingham L, Arme C (1977) Intestinal absorption of amino acids by rainbow trout, Salmo gairdneri (Richardson). J Comp Physiol B 117:323–334. doi:10.1007/BF00691558 CrossRefGoogle Scholar
  20. Kamalam BS, Panserat S, Aguirre P et al (2013) Selection for high muscle fat in rainbow trout induces potentially higher chylomicron synthesis and PUFA biosynthesis in the intestine. Comp Biochem Physiol A: Mol Integr Physiol 164:417–427. doi:10.1016/j.cbpa.2012.11.020 CrossRefGoogle Scholar
  21. Kirchner S, Panserat S, Lim PL et al (2008) The role of hepatic, renal and intestinal gluconeogenic enzymes in glucose homeostasis of juvenile rainbow trout. J Comp Physiol B Biochem Syst Environ Physiol 178:429–438. doi:10.1007/s00360-007-0235-7 CrossRefGoogle Scholar
  22. Larsen BK, Dalsgaard J, Pedersen PB (2012) Effects of plant proteins on postprandial, free plasma amino acid concentrations in rainbow trout (Oncorhynchus mykiss). Aquaculture 326–329:90–98. doi:10.1016/j.aquaculture.2011.11.028 CrossRefGoogle Scholar
  23. Lazzarotto V, Médale F, Larroquet L et al (2014) Long term feeding rainbow trout with fish meal and fish oil free diet: consequences on growth performance, whole body lipid content and fatty acid profile. In: Symposium proceedings ISFNF2014.16th international symposium on fish nutrition and feeding, May 25–30th 2014, Cairns, Australia, p 115. http://prodinra.inra.fr/record/264822
  24. Liu Z, Zhou Y, Liu S et al (2014) Characterization and dietary regulation of oligopeptide transporter (PepT1) in different ploidy fishes. Peptides 52:149–156. doi:10.1016/j.peptides.2013.12.017 CrossRefPubMedGoogle Scholar
  25. McLean E, Rønsholdt B, Sten C (1999) Gastrointestinal delivery of peptide and protein drugs to aquacultured teleosts. Aquaculture 177:231–247. doi:10.1016/S0044-8486(99)00087-3 CrossRefGoogle Scholar
  26. Moore S (1968) Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J Biol Chem 243:6281–6283. http://www.jbc.org/content/243/23/6281
  27. Naylor RL, Hardy RW, Bureau D et al (2009) Feeding aquaculture in an era of finite resources. Proc Natl Acad Sci USA 106:15103–15110. doi:10.1073/pnas.0905235106 CrossRefPubMedPubMedCentralGoogle Scholar
  28. NRC—National Research Council (2011) Nutrient requirements of fish. National Academic Press, Washington, DCGoogle Scholar
  29. Olsen RE, Myklebust R, Kaino T, Ringo E (1999) Lipid digestibility and ultrastructural changes in the enterocytes of Arctic char (Salvelinus alpinus L.) fed linseed oil and soybean lecithin. Fish Physiol Biochem 21:35–44CrossRefGoogle Scholar
  30. Olsen RE, Myklebust R, Ringo E, Mayhew TM (2000) The influences of dietary linseed oil and saturated fatty acids on caecal enterocytes in Arctic char (Salvelinus alpinus L.): a quantitative ultrastructural study. Fish Physiol Biochem 22:207–216. doi:10.1023/A:1007879127182 CrossRefGoogle Scholar
  31. Ostaszewska T, Kamaszewski M, Grochowski P et al (2010) The effect of peptide absorption on PepT1 gene expression and digestive system hormones in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A: Mol Integr Physiol 155:107–114. doi:10.1016/j.cbpa.2009.10.017 CrossRefGoogle Scholar
  32. Polakof S, Skiba-Cassy S, Kaushik S et al (2012) Glucose and lipid metabolism in the pancreas of rainbow trout is regulated at the molecular level by nutritional status and carbohydrate intake. J Comp Physiol B 182(4):507–516. doi:10.1007/s00360-011-0636-5 Epub 2011 Dec 22 CrossRefPubMedGoogle Scholar
  33. Richard N, Mourente G, Kaushik S, Corraze G (2006) Replacement of a large portion of fish oil by vegetable oils does not affect lipogenesis, lipid transport and tissue lipid uptake in European seabass (Dicentrarchus labrax L.). Aquaculture 261:1077–1087. doi:10.1016/j.aquaculture.2006.07.021 CrossRefGoogle Scholar
  34. Romo Vaquero M, Yáñez-Gascón M-J, Garcia Villalba R et al (2012) Inhibition of gastric lipase as a mechanism for body weight and plasma lipids reduction in Zucker rats fed a rosemary extract rich in carnosic acid. PLoS ONE 7(6):e39773. doi:10.1371/journal.pone.0039773 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ruohonen K, Grove DJ, McIlroy J (1997) The amount of food ingested in a single meal by rainbow trout offered chopped herring, dry and wet diets. J Fish Biol 51:93–105. doi:10.1006/jfbi.1997.0415 CrossRefPubMedGoogle Scholar
  36. Rust MB (2002) Nutritional physiology. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, San Diego, pp 454–504Google Scholar
  37. Santigosa E, Sánchez J, Médale F et al (2008) Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources. Aquaculture 282:68–74. doi:10.1016/j.aquaculture.2008.06.007 CrossRefGoogle Scholar
  38. Santigosa E, García-Meilán I, Valentin JM et al (2011) Modifications of intestinal nutrient absorption in response to dietary fish meal replacement by plant protein sources in sea bream (Sparus aurata) and rainbow trout (Onchorynchus mykiss). Aquaculture 317:146–154. doi:10.1016/j.aquaculture.2011.04.026 CrossRefGoogle Scholar
  39. Sauvant D, Perez J-M, Tran G (2004) Tables INRA-AFZ de composition et de valeur nutritive des matières premières destinées aux animaux d’élevage: porcs, volailles, bovins, ovins, caprins, lapins, chevaux, poissons. Seconde édition revue et corrigée, mars 2004, INRA Editions Versailles, 304 p. Coord. ISBN:2-7380-1046-6 2002Google Scholar
  40. Sire MF, Vernier JM (1992) Intestinal absorption of protein in teleost fish. Comp Biochem Physiol A Physiol 103:771–781. doi:10.1016/0300-9629(92)90180-X CrossRefGoogle Scholar
  41. Wøjdemann M, Riber C, Bisgaard T et al (1999) Inhibition of human gastric lipase by intraduodenal fat involves glucagon-like peptide-1 and cholecystokinin. Regul Pept 80:101–106. doi:10.1016/S0167-0115(99)00011-7 CrossRefPubMedGoogle Scholar
  42. Yamamoto T, Tatsuya U, Akiyama T (1998) Postprandial changes in plasma free amino acid concentrations of rainbow trout fed diets containing different protein sources. Fish Sci 64(3):474–481. doi:10.2331/fishsci.64.474 Google Scholar
  43. Yúfera M, Moyano FJ, Astola A et al (2012) Acidic digestion in a teleost: postprandial and circadian pattern of gastric pH, pepsin activity, and pepsinogen and proton pump mRNAs expression. PLoS ONE 7:1–9. doi:10.1371/journal.pone.0033687 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Marion Borey
    • 1
    • 2
  • Stephane Panserat
    • 1
  • Anne Surget
    • 1
  • Marianne Cluzeaud
    • 1
  • Elisabeth Plagnes-Juan
    • 1
  • Alexandre Herman
    • 1
  • Viviana Lazzarotto
    • 1
  • Geneviève Corraze
    • 1
  • Françoise Médale
    • 1
  • Beatrice Lauga
    • 2
  • Christine Burel
    • 1
  1. 1.UMR1419 Nutrition, Métabolisme, AquacultureINRASaint Pee sur NivelleFrance
  2. 2.EEM, UMR 5254 IPREM, Equipe Environnement et MicrobiologieUniversité de Pau et des Pays de l’AdourPauFrance

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