Exploring the Impact of a Low-Protein High-Carbohydrate Diet in Mature Broodstock of a Glucose-Intolerant Teleost, the Rainbow Trout

Sustainable aquaculture production requires a greater reduction in the use of marine-derived ingredients, and one of the most promising solutions today is the augmentation in the proportion of digestible carbohydrates in aquafeed. This challenge is particularly difficult for high trophic level teleo...

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Main Authors: Thérèse Callet, Huihua Hu, Laurence Larroquet, Anne Surget, Jingwei Liu, Elisabeth Plagnes-Juan, Patrick Maunas, Nicolas Turonnet, Jan Alexander Mennigen, Julien Bobe, Christine Burel, Geneviève Corraze, Stephane Panserat, Lucie Marandel
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fphys.2020.00303/full
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author Thérèse Callet
Huihua Hu
Huihua Hu
Huihua Hu
Laurence Larroquet
Anne Surget
Jingwei Liu
Elisabeth Plagnes-Juan
Patrick Maunas
Nicolas Turonnet
Jan Alexander Mennigen
Julien Bobe
Christine Burel
Geneviève Corraze
Stephane Panserat
Lucie Marandel
author_facet Thérèse Callet
Huihua Hu
Huihua Hu
Huihua Hu
Laurence Larroquet
Anne Surget
Jingwei Liu
Elisabeth Plagnes-Juan
Patrick Maunas
Nicolas Turonnet
Jan Alexander Mennigen
Julien Bobe
Christine Burel
Geneviève Corraze
Stephane Panserat
Lucie Marandel
author_sort Thérèse Callet
collection DOAJ
description Sustainable aquaculture production requires a greater reduction in the use of marine-derived ingredients, and one of the most promising solutions today is the augmentation in the proportion of digestible carbohydrates in aquafeed. This challenge is particularly difficult for high trophic level teleost fish as they are considered to be glucose-intolerant (growth delay and persistent postprandial hyperglycemia observed in juveniles fed a diet containing more than 20% of carbohydrates). It was previously suggested that broodstock could potentially use carbohydrates more efficiently than juveniles, probably due to important metabolic changes that occur during gametogenesis. To investigate this hypothesis, 2-year old male and female rainbow trout (Oncorhynchus mykiss) were either fed a diet containing no carbohydrates (NC) or a 35%-carbohydrate diet (HC) for an entire reproductive cycle. Zootechnical parameters as well as the activities of enzymes involved in carbohydrate metabolism were measured in livers and gonads. Fish were then reproduced to investigate the effects of such a diet on reproductive performance. Broodstock consumed the HC diet, and in contrast to what is commonly observed in juveniles, they were able to grow normally and they did not display postprandial hyperglycemia. The modulation of their hepatic metabolism, with an augmentation of the glycogenesis, the pentose phosphate pathway and a possible better regulation of gluconeogenesis, may explain their improved ability to use dietary carbohydrates. Although the HC diet did induce precocious maturation, the reproductive performance of fish was not affected, confirming that broodstock are able to reproduce when fed a low-protein high-carbohydrate diet. In conclusion, this exploratory work has shown that broodstock are able to use a diet containing digestible carbohydrates as high as 35% and can then grow and reproduce normally over an entire reproductive cycle for females and at least at the beginning of the cycle for males. These results are highly promising and suggest that dietary carbohydrates can at least partially replace proteins in broodstock aquafeed.
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spelling doaj.art-fd4c1848f932419faa7134dd83c811792022-12-21T22:55:42ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-05-011110.3389/fphys.2020.00303518302Exploring the Impact of a Low-Protein High-Carbohydrate Diet in Mature Broodstock of a Glucose-Intolerant Teleost, the Rainbow TroutThérèse Callet0Huihua Hu1Huihua Hu2Huihua Hu3Laurence Larroquet4Anne Surget5Jingwei Liu6Elisabeth Plagnes-Juan7Patrick Maunas8Nicolas Turonnet9Jan Alexander Mennigen10Julien Bobe11Christine Burel12Geneviève Corraze13Stephane Panserat14Lucie Marandel15INRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaUniversity of the Chinese Academy of Sciences, Beijing, ChinaINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceDepartment of Biology, University of Ottawa, Ottawa, ON, CanadaINRAE, LPGP UR1037, Campus de Beaulieu, Rennes, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de l’Adour, E2S UPPA, NUMEA, Saint-Pée-sur-Nivelle, FranceSustainable aquaculture production requires a greater reduction in the use of marine-derived ingredients, and one of the most promising solutions today is the augmentation in the proportion of digestible carbohydrates in aquafeed. This challenge is particularly difficult for high trophic level teleost fish as they are considered to be glucose-intolerant (growth delay and persistent postprandial hyperglycemia observed in juveniles fed a diet containing more than 20% of carbohydrates). It was previously suggested that broodstock could potentially use carbohydrates more efficiently than juveniles, probably due to important metabolic changes that occur during gametogenesis. To investigate this hypothesis, 2-year old male and female rainbow trout (Oncorhynchus mykiss) were either fed a diet containing no carbohydrates (NC) or a 35%-carbohydrate diet (HC) for an entire reproductive cycle. Zootechnical parameters as well as the activities of enzymes involved in carbohydrate metabolism were measured in livers and gonads. Fish were then reproduced to investigate the effects of such a diet on reproductive performance. Broodstock consumed the HC diet, and in contrast to what is commonly observed in juveniles, they were able to grow normally and they did not display postprandial hyperglycemia. The modulation of their hepatic metabolism, with an augmentation of the glycogenesis, the pentose phosphate pathway and a possible better regulation of gluconeogenesis, may explain their improved ability to use dietary carbohydrates. Although the HC diet did induce precocious maturation, the reproductive performance of fish was not affected, confirming that broodstock are able to reproduce when fed a low-protein high-carbohydrate diet. In conclusion, this exploratory work has shown that broodstock are able to use a diet containing digestible carbohydrates as high as 35% and can then grow and reproduce normally over an entire reproductive cycle for females and at least at the beginning of the cycle for males. These results are highly promising and suggest that dietary carbohydrates can at least partially replace proteins in broodstock aquafeed.https://www.frontiersin.org/article/10.3389/fphys.2020.00303/fulllivergonadenzymatic activityglucose metabolismpentose phosphate pathwayglycogen
spellingShingle Thérèse Callet
Huihua Hu
Huihua Hu
Huihua Hu
Laurence Larroquet
Anne Surget
Jingwei Liu
Elisabeth Plagnes-Juan
Patrick Maunas
Nicolas Turonnet
Jan Alexander Mennigen
Julien Bobe
Christine Burel
Geneviève Corraze
Stephane Panserat
Lucie Marandel
Exploring the Impact of a Low-Protein High-Carbohydrate Diet in Mature Broodstock of a Glucose-Intolerant Teleost, the Rainbow Trout
Frontiers in Physiology
liver
gonad
enzymatic activity
glucose metabolism
pentose phosphate pathway
glycogen
title Exploring the Impact of a Low-Protein High-Carbohydrate Diet in Mature Broodstock of a Glucose-Intolerant Teleost, the Rainbow Trout
title_full Exploring the Impact of a Low-Protein High-Carbohydrate Diet in Mature Broodstock of a Glucose-Intolerant Teleost, the Rainbow Trout
title_fullStr Exploring the Impact of a Low-Protein High-Carbohydrate Diet in Mature Broodstock of a Glucose-Intolerant Teleost, the Rainbow Trout
title_full_unstemmed Exploring the Impact of a Low-Protein High-Carbohydrate Diet in Mature Broodstock of a Glucose-Intolerant Teleost, the Rainbow Trout
title_short Exploring the Impact of a Low-Protein High-Carbohydrate Diet in Mature Broodstock of a Glucose-Intolerant Teleost, the Rainbow Trout
title_sort exploring the impact of a low protein high carbohydrate diet in mature broodstock of a glucose intolerant teleost the rainbow trout
topic liver
gonad
enzymatic activity
glucose metabolism
pentose phosphate pathway
glycogen
url https://www.frontiersin.org/article/10.3389/fphys.2020.00303/full
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