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Putative imbalanced amino acid metabolism in rainbow trout long term fed a plant-based diet as revealed by ¹H-NMR metabolomics.

ABSTRACT: The long-term effect of a plant (P)-based diet was assessed by proton nuclear magnetic resonance (¹H-NMR) metabolomics in rainbow trout fed a marine fish meal (FM)-fish oil (FO) diet (M), a P-based diet and a control commercial-like diet (C) starting with the first feeding. Growth performances were not heavily altered by long-term feeding on the P-based diet. An ¹H-NMR metabolomic analysis of the feed revealed significantly different soluble chemical compound profiles between the diets. A set of soluble chemical compounds was found to be specific either to the P-based diet or to the M diet. Pterin, a biomarker of plant feedstuffs, was identified both in the P-based diet and in the plasma of fish fed the P-based diet. ¹H-NMR metabolomic analysis on fish plasma and liver and muscle tissues at 6 and 48 h post feeding revealed significantly different profiles between the P-based diet and the M diet, while the C diet showed intermediate results. A higher amino acid content was found in the plasma of fish fed the P-based diet compared with the M diet after 48 h, suggesting either a delayed delivery of the amino acids or a lower amino acid utilisation in the P-based diet. This was associated with an accumulation of essential amino acids and the depletion of glutamine in the muscle, together with an accumulation of choline in the liver. Combined with an anticipated absorption of methionine and lysine supplemented in free form, the present results suggest an imbalanced essential amino acid supply for protein metabolism in the muscle and for specific functions of the liver.

SUBMITTER: Deborde C

PROVIDER: S-EPMC8057518 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

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Putative imbalanced amino acid metabolism in rainbow trout long term fed a plant-based diet as revealed by ¹H-NMR metabolomics.

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Putative imbalanced amino acid metabolism in rainbow trout long term fed a plant-based diet as revealed by ¹H-NMR metabolomics.