Carbohydrates and fish larval nutritional programming
Contents1. Poor carbohydrates utilization in fishes and consequences in fish nutrition2. Examples of low carbohydrates and glucose utilization in fishes3. Several hypothesis that explain the phenomenon4. New explanation of the phenomenon by randle’s cycle5. New explanation of the phenomenon by glicolysis inhibition by PUFA6. Increase glucose utilization capacity in fish by glucose early programming7. Conclusion
Higher feed cost Higher water pollution Better carbohydrates utilization will increase protein sparing hence it will present economical and environmental advantagesOK !
The graphics show:a. Blood glucose higher in carnivorous than herbivorous fishesb. Plasma insulin higher in carnivorous than herbivorous fishesc. Phosphofructokinase higher in herbivorous than carnivorous fishes
Plasma glucose decrease below 100 mg/dlonly after 8 hours in carnivorous fish.
Species Carbohydrates digestion Glucose utilisation Less ability but prefer to low amylopectin-containedAsian seabass (Lates calcarifer) Poor (4) and gelatinized starch (1–3)Atlantic halibut (Hippoglossus Less active amylase (5) Poor, but 5%-8% better than 2% (5)hippoglossus) Poor, but prefer to low level (<16%) (6) &Atlantic salmon (Salmo salar) Less active amylase (6) higher temperature (180C) (7) Digest gelatinized starch up to 80% for <24,2% in feedCobia (Rachycentron canadum) Low utilized (9) (8)European seabass (Dicentrachus Less amylolytic activity, suggested concentration <30% Poor (prolonged hyperglycemia) (10)labrax) in diet (10) Better amylolitic activity, better digest wheat andGilthead seabream (Sparus aurata) Restore plasma glucose after 12 h (14) extruded source (11–13) Prefer starch than glucose (E. malabaricus, E. coioides) Protein sparing at low protein diet (E.Grouper (15, 16) malabaricus) (17)Japanese flounder (Paralichthyis Utilize dextrin better than cellulose, maltose, glucoseolivaceus) Hyperglycemia 16-24 h (18) (18)Rainbow trout (Onchorynchus Low digestible (19–21) Poor (22–25)mykiss)Red drum (Sciaenops ocellatus) Low digestible but prefer complex starch (26) Low utilized (26)Red seabream (Pagrus major) Low digestible (27, 28) Low utilized compared to lipid (29, 30)Southern bluefin tuna (Thunnus Assumed to be low digestible because low amylase -maccoyii) present (31–33) Low digestible but prefer complex starch (10%-20% Low restore because low plasma insulinYellowtail (Seriola quinquerradiata) diet) (34, 35) level (35)
Low concentration digestive enzymes (Helland and Helland, 2002)Short gut intestine (Drew et al 2004)Glucose low stimulate insulin secretion (Mommsen et al, 1991)The relatively low number of insulin receptors in fish muscle as compared to the rat(Pa´rrizas et al. 1994)Low number of glucose transporters in fish muscle (Wright et al. 1998)A low glucose phosphorylation capacity (Cowey and Walton 1989)An imbalance between hepatic glucose uptake and endogenous production(Panserat et al. 2001a)
Explanation for low glucose utilization by Enes et al (2009)1. Data strongly suggest that the liver of most fish species is apparently capable of regulating glucose storage2. However, endogenous glucose production is still high whether fish is in feeding or fasting state.3. This endogenous glucose production leads a putative competition with exogenous (dietary) glucose.4. This may explain the poor glucose utilization in fish (Enes et al. 2009)But why is endogenous glucose production highly persistent ?New explanation may be found here:1. Gluconeogenesis could be induced by fatty acid oxidation (Randle, 1988)2. Fatty acid oxidation could be induced by PUFA rich diet (Clarke, 2001)
Utilization of fatty acid as energy source Utilization of glucose as energy sourceprevent glucose utilization prevent triacyl glycerol breakdown
Fatty acids that have two or more double bondslinoleic acid (LA)γ-linolenic acid (GLA)arachidonic acid (AA)Alpha-linolenic acid (ALA)Eicosapentaenoic acid (EPA)Docosahexaenoic acid (DHA)
(Delarue et al., 2004; Ghafoorunissa et al., 2005; Postic et al., 2007; Fedor and Kelley, 2009;González-Périz et al., 2009) PUFA Can not cure insulin resistance Its only Prevent insulin resistance by reduce lipid deposition 1. Decrease lipogenesis and glicolysis 2. Increase lipolysis and beta oxidation and gluconeogenesis
PUFA PREVENT TRANSCRIPTIONBY INHIBIT ChREBP (GLYCOLISIS) AND SREBP1-C (LIPOGENESIS) (Postic et al. 2007)
1. Reducing the nuclear abundance and DNA-binding affinity of transcription factors responsible for imparting insulin and carbohydrate control to lipogenic and glycolytic genes.2. In particular, PUFA suppress the nuclear abundance and expression of sterol regulatory element binding protein-1 and reduce the DNA-binding activities of nuclear factor Y, Sp1 and possibly hepatic nuclear factor-4
The higher rates of fatty acid oxidation observed in humans and animals fed dietsrich in PUFA (Clark, 2001)Oxidation of fatty acids and ketone bodies inhibit glucose metabolism in cardiacand red skeletal muscle and induce gluconeogenesis (Randle, 1988)Utilizing lipid simultaneously as energy source impairs insulin response by glucose(Randle, 1998)Fish prolonged uptake PUFA, hence simultaneously use to fatty acid asrespiratory substrates, induce gluconeogenesis finally impairs insulinresponse and may have implication in metabolic inflexibility.
Nutritional programming1. Specific fish habitat provide particular feeds that may naturally contain specific food composition. They consume these kinds of feeds continuously.2. Fish adapt efficiently to this condition by performing certain metabolic pathway more often than the others. It means some genes express more frequent than the others. Afterward , this state become fish habit.3. It could be changed by early programming of larvae. They are conditioned simultaneously by particular set of nutritional state that induce desired gene expression relates to specific metabolic pathway.4. Consequently this metabolic state is still continued in the latter of fish live stage.
Nutritional Programming for glucose utilization (Geurden et al 2007)Based on the concept of nutritional programming in higher vertebrates, it was tested whether an acute hyperglucidicstimulus during early life could induce a long-lasting effect on carbohydrate utilization in carnivorous rainbow trout.1. hyperglucidic diet (60% dextrin) at two early stages of development: either at first feeding (3 days, stimulus 1) or after yolk absorption (5 days, stimulus 2).2. Before and after the hyperglucidic stimulus, they received a commercial diet until juvenile stage (>10 g).3. Fish that did not experience the hyperglucidic stimuli served as controls.4. The short- and long-term effects of the stimuli were evaluated by measuring the expression of five key genes involved in carbohydrate utilization: α-amylase, maltase (digestion), sodium-dependent glucose cotransporter (SGLT1; intestinal glucose transport), and glucokinase and glucose-6-phosphatase, involved in the utilization and production of glucose, respectively.5. The hyperglucidic diet rapidly increased expressions of maltase, α-amylase, and glucokinase in stimulus 1 fish and only of maltase in stimulus 2 fish, probably because of a lower plasticity at this later stage of development.6. In the final challenge test with juveniles fed a 25% dextrin diet, both digestive enzymes were upregulated in fish that had experienced the hyperglucidic stimulus at first feeding, confirming the possibility of modification of some long-term physiological functions in rainbow trout.7. In contrast, no persistent molecular adaptations were found for the genes involved in glucose transport or metabolism. In addition, growth and postprandial glycemia were unaffected by the stimuli.8. In summary, data show that a short hyperglucidic stimulus during early trout life may permanently influence carbohydrate digestion.
Conclusion1. Many evidences show that fishes utilize carbohydrates and glucose poorly2. Carnivorous fishes are lower utilize carbohydrates than the herbivorous3. Several hypothesis that explain the phenomenon still raise many questions4. Randle’s cycle explain more clearly that glucose utilization is inhibited by fatty acid utilization.5. Inhibition of glucose utilization much more plainly by glicolysis inhibition by PUFA6. In certain level, glucose utilization capability in fish could be increased by early programming7. Conclusion
References:1. Glencross, B., Blyth, D., Tabrett, S., Bourne, N., Irvin, S., Anderson, M., Fox‐smith, T., and Smullen, R. (2011) An assessment of cereal grains and other starch sources in diets for barramundi (Lates calcarifer) – implications for nutritional and functional qualities of extruded feeds, Aquaculture Nutrition 1-12.2. Boonyaratpalin, M., and Williams, K. (2002) Asian seabass (Lates calcarifer). In Nutrient Requirements and Feeding of Finfish for Aquaculture (Webster, C. D., and Lim, C. E., Eds.) First., CABI.3. Mali, B. (1997) Nutrient requirements of marine food fish cultured in Southeast Asia, Aquaculture 151, 283-313.4. Glencross, B. (2006) The nutritional management of barramundi, Lates calcarifer– a review, Aquaculture Nutrition 12, 291-309.5. Helland, B. G., and Helland, S. J. (2002) Atlantic halibut (Hippoglossus hippoglossus). In Nutrient Requirements and Feeding of Finfish for Aquaculture (Webster, C. D., and Lim, C. E., Eds.) First., CABI.6. Storebakken, T. (2002) Atlantic salmon (Salmo salar). In Nutrient Requirements and Feeding of Finfish for Aquaculture (Webster, C. D., and Lim, C. E., Eds.) First., CABI.7. Papoutsoglou, E. S., and Lyndon, A. R. (2005) Effect of incubation temperature on carbohydrate digestion in important teleosts for aquaculture, Aquaculture Research 36, 1252-1264.8. Ren, M., Ai, Q., Mai, K., Ma, H., and Wang, X. (2011) Effect of dietary carbohydrate level on growth performance, body composition, apparent digestibility coefficient and digestive enzyme activities of juvenile cobia, Rachycentron canadum L, Aquaculture Research 42, 1467-1475.9. Jr Webb, K. a, Rawlinson, L. t, and Holt, G. j. (2010) Effects of dietary starches and the protein to energy ratio on growth and feed efficiency of juvenile cobia, Rachycentron canadum, Aquaculture Nutrition 16, 447-456.10. Kaushik, S. J. (2002) European seabass (Dicentrachus labrax). In Nutrient Requirements and Feeding of Finfish for Aquaculture (Webster, C. D., and Lim, C. E., Eds.) First., CABI.11. Munilla-Morán, R., and Saborido-Rey, F. (1996) Digestive enzymes in marine species. II. Amylase activities in gut from seabream (Sparus aurata), turbot (Scophthalmus maximus) and redfish (Sebastes mentella), Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 113, 827-834.12. Venou, B., Alexis, M. N., Fountoulaki, E., Nengas, I., Apostolopoulou, M., and Castritsi-Cathariou, I. (2003) Effect of extrusion of wheat and corn on gilthead sea bream (Sparus aurata) growth, nutrient utilization efficiency, rates of gastric evacuation and digestive enzyme activities, Aquaculture 225, 207-223.13. Lupatsch, I., Kissil, G. W., Sklan, D., and Pfeffer, E. (1997) Apparent digestibility coefficients of feed ingredients and their predictability in compound diets for gilthead seabream, Sparus aurata L., Aquaculture Nutrition 3, 81-89.14. Enes, P., Panserat, S., Kaushik, S., and Oliva-Teles, A. (2011) Dietary Carbohydrate Utilization by European Sea Bass (Dicentrarchus labrax L.) and Gilthead Sea Bream (Sparus aurata L.) Juveniles, Reviews in Fisheries Science 19, 201-215.15. Shiau, S., and Lin, Y. (2002) Utilization of glucose and starch by the grouper Epinephelus malabaricus at 23°C, Fisheries Science 68, 991-995.
16. Eusebio, P. S., Coloso, R. M., and Mamauag, R. E. P. (2004) Apparent digestibility of selected ingredients in diets for juvenile grouper, Epinephelus coioides (Hamilton), Aquaculture Research 35, 1261-1269.17. Shiau, S., and Lin, Y. (2001) Carbohydrate utilization and its protein-sparing effect in diets for grouper (Epinephelus malabaricus), Animal Science-Glasgow 73, 299–304.18. Lee, S.-M., Kim, K.-D., and Lall, S. P. (2003) Utilization of glucose, maltose, dextrin and cellulose by juvenile flounder (Paralichthys olivaceus), Aquaculture 221, 427-438.19. Francoise, B. (1979) Carbohydrate in rainbow trout diets: Effects of the level and source of carbohydrate and the number of meals on growth and body composition, Aquaculture 18, 157-167.20. Spannhof, L., and Plantikow, H. (1983) Studies on carbohydrate digestion in rainbow trout, Aquaculture 30, 95-108.21. Felip, O., Ibarz, A., Fernández-Borràs, J., Beltrán, M., Martín-Pérez, M., Planas, J. V., and Blasco, J. (2011) Tracing Metabolic Routes of Dietary Carbohydrate and Protein in Rainbow Trout (Oncorhynchus Mykiss) Using Stable Isotopes ([13C]starch and [15N]protein): Effects of Gelatinisation of Starches and Sustained Swimming, British Journal of Nutrition FirstView, 1-11.22. Kaushik, S. J., Medale, F., Fauconneau, B., and Blanc, D. (1989) Effect of digestible carbohydrates on protein/energy utilization and on glucose metabolism in rainbow trout (Salmo gairdneri R.), Aquaculture 79, 63-74.23. Françoise, B. (1979) Effects of dietary carbohydrates and of their mode of distribution on glycaemia in rainbow trout (Salmo gairdneri richardson), Comparative Biochemistry and Physiology Part A: Physiology 64, 543-547.24. Panserat, S., Capilla, E., Gutierrez, J., Frappart, P. O., Vachot, C., Plagnes-Juan, E., Aguirre, P., Brèque, J., and Kaushik, S. (2001) Glucokinase is highly induced and glucose-6-phosphatase poorly repressed in liver of rainbow trout (Oncorhynchus mykiss) by a single meal with glucose, Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 128, 275-283.25. Legate, N. J., Bonen, A., and Moon, T. W. (2001) Glucose Tolerance and Peripheral Glucose Utilization in Rainbow Trout (Oncorhynchus mykiss), American Eel (Anguilla rostrata), and Black Bullhead Catfish (Ameiurus melas), General and Comparative Endocrinology 122, 48-59.26. Koshio, S. (2002) Red seabream (Pagrus major). In Nutrient Requirements and Feeding of Finfish for Aquaculture (Webster, C. D., and Lim, C. E., Eds.) First., CABI.27. McGoogan, B. B., and Reigh, R. C. (1996) Apparent digestibility of selected ingredients in red drum (Sciaenops ocellatus) diets, Aquaculture 141, 233-244.28. Gaylord, T. G., and Gatlin III, D. M. (1996) Determination of digestibility coefficients of various feedstuffs for red drum (Sciaenops ocellatus), Aquaculture 139, 303-314.29. Serrano, J. A., Nematipour, G. R., and Gatlin III, D. M. (1992) Dietary protein requirement of the red drum (Sciaenops ocellatus) and relative use of dietary carbohydrate and lipid, Aquaculture 101, 283-291.30. Ellis, S. C., and Reigh, R. C. (1991) Effects of dietary lipid and carbohydrate levels on growth and body composition of juvenile red drum, Sciaenops ocellatus, Aquaculture 97, 383-394.
31. Kaushik, S. J. (2002) Southern bluefin tuna (Thunnus maccoyii). In Nutrient Requirements and Feeding of Finfish for Aquaculture (Webster, C. D., and Lim, C. E., Eds.) First., CABI.32. Parra, A. M., Rosas, A., Lazo, J. P., and Viana, M. T. (2007) Partial characterization of the digestive enzymes of Pacific bluefin tuna Thunnus orientalis under culture conditions, Fish Physiology and Biochemistry 33, 223-231.33. Mourente, G., and Tocher, D. R. (2003) An approach to study the nutritional requirements of the bluefin tuna (Thunnus thynnus thynnus L.), CIHEAM-IAMZ 60, 143 - 150.34. Watanabe, T., Aoki, H., Watanabe, K., Maita, M., Yamagata, Y., and Satoh, S. (2001) Quality evaluation of different types of non‐fish meal diets for yellowtail, Fisheries Science 67, 461-469.35. Masumoto, T. (2002) Yellowtail (Seriola quinquerradiata). In Nutrient Requirements and Feeding of Finfish for Aquaculture (Webster, C. D., and Lim, C. E., Eds.) First., CABI.
References for the new hypothesisAalinkeel, R., M. Srinivasan, F. Song, and M.S. Patel. 2001. Programming into adulthood of islet adaptations induced by early nutritional intervention in the rat. Am J Physiol Endocrinol Metab 281(3): E640–E648.Clarke, S.D. 2001. Polyunsaturated Fatty Acid Regulation of Gene Transcription: A Molecular Mechanism to Improve the Metabolic Syndrome. The Journal of Nutrition 131(4): 1129 –1132.Enes, P., S. Panserat, S. Kaushik, and A. Oliva-Teles. 2008. Nutritional regulation of hepatic glucose metabolism in fish. Fish Physiology and Biochemistry 35(3): 519–539.Geurden, I., M. Aramendi, J. Zambonino-Infante, and S. Panserat. 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(6): R2275–R2283.Hue, L., and H. Taegtmeyer. 2009. The Randle cycle revisited: a new head for an old hat. American Journal of Physiology - Endocrinology And Metabolism 297(3): E578 –E591.Postic, C., R. Dentin, P.-D. Denechaud, and J. Girard. 2007. ChREBP, a Transcriptional Regulator of Glucose and Lipid Metabolism. Annual Review of Nutrition 27(1): 179–192.Poupeau, A., and C. Postic. 2011. Cross-regulation of hepatic glucose metabolism via ChREBP and nuclear receptors. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease 1812(8): 995–1006.Randle, P. 1998. Regulatory interactions between lipids and carbohydrates: The glucose fatty acid cycle after 35 years. Diabetes-Metab. Rev. 14(4): 263–283.Voet, D., J.G. Voet, and C.W. Pratt. 2008. Fundamentals of Biochemistry: Life at the Molecular Level. 3rd ed. Wiley, USA.