Dataset Information

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

ABSTRACT: 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.

SUBMITTER: Callet T

PROVIDER: S-EPMC7243711 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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

Callet Thérèse T Hu Huihua H Larroquet Laurence L Surget Anne A Liu Jingwei J Plagnes-Juan Elisabeth E Maunas Patrick P Turonnet Nicolas N Mennigen Jan Alexander JA Bobe Julien J Burel Christine C Corraze Geneviève G Panserat Stephane S Marandel Lucie L

Frontiers in physiology 20200515

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 prev ...[more]

PMID: 32499714

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Project description:Purpose: Next-generation sequencing (NGS) of small RNAs allows transcriptome level analysis of the miRNAome. The goals of this study are to identify differentially regulated hepatic miRNAs in response to a diet with high (>20%) or low (0%) carbohydrate content following a short term fast using small RNA next generation sequencing. Specific quantitative reverse transcription polymerase chain reaction (qRT–PCR) methods were used to validate optimal high-throughput data analysis, and in silico prediction to identify bona fide target pathways regulated by differentially regulated miRNAs following these nutritional stimuli. Method: Small RNA sequencing was performed using four randomly selected samples from each treatment group were used for sequencing. The quality of total RNA was confirmed by RNA Integrity Numbers greater than 9.0 using an Agilent Technologies 2100 Bioanalyzer. Nucleotide fractions (15-50) of small RNA were isolated from the total RNA using polyacrylamide gel electrophoresis and were ligated to a 30 adapter followed by a 50 adapter (Illumina, San Diego, CA, USA). The small RNA ligated to the adaptors was reverse transcribed to cDNA, PCR amplified and gel purified. The gel-extracted cDNA was used for library preparation, which was further used for cluster generation on Illumina's Cluster Station before sequencing using Illumina GAIIx. Raw sequence data was obtained from image data using Illumina's Sequencing Control Studio software version 2.8 (SCS v2.8) following real-time sequencing image analysis and base-calling by Illumina's Real-Time Analysis version 1.8.70 (RTA v1.8.70). The ACGT101-miR v4.2 pipeline (LC Sciences) was used to analyze sequenced data. Sequences with low Q scores, reads mapped to mRNA, RFam, Repbase and piRNA database were deleted and unique families were generated from identical sequences. These filtered unique sequences were then mapped to fish pre-miRNA and miRNA using miRBase or to the rainbow trout genome (Berthelot et al., 2014) to identify conserved miRNA following ACGT-101 User's Manual. Unique or novel miRNAs were identified after the BLAST performed against fish miRNAs from miRbase database (release 21) and published miRNAs from rainbow trout (Mennigen et al., 2016). The miRNAs that do not match any sequences in the specified databases and have the propensity of forming hairpin structure with the extended sequences at the mapped positions were classified as unique miRNAs. These unique miRNAs were further classified into different groups depending on the mappable reads to selected miRNAs in miRbase. Differentially expressed miRNAs were identified using the statistical software R (Version 3.2.2) package DESeq2 for one-way ANOVA comparison of all three treatment groups. Real-time RT–PCR validation was performed using SYBR Green assays Results: Refeeding differentially regulates hepatic miRNA abundance in a diet dependent manner: In trout refed with a low (0%) CHO diet, refeeding resulted in the 23 differntiaally regulated miRNA, of which 17 miRNAs were upregulated and 6 miRNAs were downregulated. In trout refed with a high (>20%) CHO diet, refeeding resulted in 49 differentially regulated miRNA, of which 20 miRNAs were upregulated and 29 miRNA were downregulated. Irrespecitve of the diet, 5 miRNAs were commonly regulated by refeeding alone, 4 miRNAs were upregulated and 1 was downregulated. When comparing hepatic miRNA profiles in trout following refeeding, there were 30 miRNAs that were differntially regulated after refeeding with different diets, 16 miRNAs were upregulated with the high CHO diet while 14 miRNAs were downregulated with the high CHO diet. Conclusions: Our study represents the first detailed analysis of the rainbow trout miRNAome in response to nutritional stimuli. Specifically, we here identify common hepatic miRNAs differentially regulated by refeeding following a short-term fast (2d), as well as miRNAs differentially regulated in the postprandial state depending on the dieatary stimulus (no carbohydrates compared to >20% dietary carbohydrates)

Project description:BackgroundGenomic analyses have the potential to impact selective breeding programs by identifying markers that serve as proxies for traits which are expensive or difficult to measure. Also, identifying genes affecting traits of interest enhances our understanding of their underlying biochemical pathways. To this end we conducted genome scans of seven rainbow trout families from a single broodstock population to identify quantitative trait loci (QTL) having an effect on stress response to crowding as measured by plasma cortisol concentration. Our goal was to estimate the number of major genes having large effects on this trait in our broodstock population through the identification of QTL.ResultsA genome scan including 380 microsatellite markers representing 29 chromosomes resulted in the de novo construction of genetic maps which were in good agreement with the NCCCWA genetic map. Unique sets of QTL were detected for two traits which were defined after observing a low correlation between repeated measurements of plasma cortisol concentration in response to stress. A highly significant QTL was detected in three independent analyses on Omy16, many additional suggestive and significant QTL were also identified. With linkage-based methods of QTL analysis such as half-sib regression interval mapping and a variance component method, we determined that the significant and suggestive QTL explain about 40-43% and 13-27% of the phenotypic trait variation, respectively.ConclusionsThe cortisol response to crowding stress is a complex trait controlled in a sub-sample of our broodstock population by multiple QTL on at least 8 chromosomes. These QTL are largely different from others previously identified for a similar trait, documenting that population specific genetic variants independently affect cortisol response in ways that may result in different impacts on growth. Also, mapping QTL for multiple traits associated with stress response detected trait specific QTL which indicate the significance of the first plasma cortisol measurement in defining the trait. Fine mapping these QTL can lead towards the identification of genes affecting stress response and may influence approaches to selection for this economically important stress response trait.

Project description:BackgroundHigh dietary carbohydrates can spare protein in rainbow trout (Oncorhynchus mykiss) but may affect growth and health. Inulin, a prebiotic, could have nutritional and metabolic effects, along with anti-inflammatory properties in teleosts, improving growth and welfare. We tested this hypothesis in rainbow trout by feeding them a 100% plant-based diet, which is a viable alternative to fishmeal and fish oil in aquaculture feeds. In a two-factor design, we examined the impact of inulin (2%) as well as the variation in the carbohydrates (CHO)/plant protein ratio on rainbow trout. We assessed the influence of these factors on zootechnical parameters, plasma metabolites, gut microbiota, production of short-chain fatty acids and lactic acid, as well as the expression of free-fatty acid receptor genes in the mid-intestine, intermediary liver metabolism, and immune markers in a 12-week feeding trial.ResultsThe use of 2% inulin did not significantly change the fish intestinal microbiota, but interestingly, the high CHO/protein ratio group showed a change in intestinal microbiota and in particular the beta diversity, with 21 bacterial genera affected, including Ralstonia, Bacillus, and 11 lactic-acid producing bacteria. There were higher levels of butyric, and valeric acid in groups fed with high CHO/protein diet but not with inulin. The high CHO/protein group showed a decrease in the expression of pro-inflammatory cytokines (il1b, il8, and tnfa) in liver and a lower expression of the genes coding for tight-junction proteins in mid-intestine (tjp1a and tjp3). However, the 2% inulin did not modify the expression of plasma immune markers. Finally, inulin induced a negative effect on rainbow trout growth performance irrespective of the dietary carbohydrates.ConclusionsWith a 100% plant-based diet, inclusion of high levels of carbohydrates could be a promising way for fish nutrition in aquaculture through a protein sparing effect whereas the supplementation of 2% inulin does not appear to improve the use of CHO when combined with a 100% plant-based diet.

Project description:Carnivorous rainbow trout exhibit prolonged postprandial hyperglycemia when fed a diet exceeding 20% carbohydrate content. This poor capacity to utilize carbohydrates has led to rainbow trout being classified as "glucose-intolerant" (GI). The metabolic phenotype has spurred research to identify the underlying cellular and molecular mechanisms of glucose intolerance, largely because carbohydrate-rich diets provide economic and ecological advantages over traditionally used fish meal, considered unsustainable for rainbow trout aquaculture operations. Evidence points to a contribution of hepatic intermediary carbohydrate and lipid metabolism, as well as upstream insulin signaling. Recently, microRNAs (miRNAs), small noncoding RNAs acting as negative posttranscriptional regulators affecting target mRNA stability and translation, have emerged as critical regulators of hepatic control of glucose-homeostasis in mammals, revealing that dysregulated hepatic miRNAs might play a role in organismal hyperglycemia in metabolic disease. To determine whether hepatic regulatory miRNA networks may contribute to GI in rainbow trout, we induced prolonged postprandial hyperglycemia in rainbow trout by using a carbohydrate-rich diet and profiled genome-wide hepatic miRNAs in hyperglycemic rainbow trout compared with fasted trout and trout fed a diet devoid of carbohydrates. Using small RNA next-generation sequencing and real-time RT-PCR validation, we identified differentially regulated hepatic miRNAs between these groups and used an in silico approach to predict bona fide mRNA targets and enriched pathways. Diet-induced hyperglycemia resulted in differential regulation of hepatic miRNAs compared with fasted fish. Some of the identified miRNAs, such as miRNA-27b-3p and miRNA-200a-3p, are known to be responsive to hyperglycemia in the liver of hyperglycemic glucose-tolerant fish and mammals, suggesting an evolutionary conserved regulation. Using Gene Ontology term-based enrichment analysis, we identify intermediate carbohydrate and lipid metabolism and insulin signaling as potential targets of posttranscriptional regulation by hyperglycemia-regulated miRNAs and provide correlative expression analysis of specific predicted miRNA-target pairs. This study identifies hepatic miRNAs in rainbow trout that exhibit differential postprandial expression in response to diets with different carbohydrate content and predicts posttranscriptionally regulated target mRNAs enriched for pathways involved in glucoregulation. Together, these results provide a framework for testable hypotheses of functional involvement of specific hepatic miRNAs in GI in rainbow trout.

Dataset Information

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

Publications

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

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