Background High 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. Results The 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. Conclusions With 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.

Short-term adaptation of the microbiota could promote nutrient degradation and the host health. While numerous studies are currently undertaking feeding trials using sustainable diets for the aquaculture industry, the extent to which the microbiota adapts to these novel diets is poorly described. The incorporation of carbohydrates (CHO) within a 100% plant-based diet could offer a novel, cost-effective energy source that is readily available, potentially replacing the protein component in the diets. In this study, we investigated the short-term (3 weeks) effects of a high CHO, 100% plant-based diet on the mucosal and digesta associated microbiota diversity and composition, as well as several metabolic parameters in rainbow trout. We highlighted that the mucosa is dominated by Mycoplasma (44.86%). While the diets did not have significant effects on the main phyla (Proteobacteria, Firmicutes, and Actinobacteria), after 3 weeks, a lower abundance of Bacillus genus, and higher abundances of four lactic-acid bacteria were demonstrated in digesta. In addition, no post-prandial hyperglycemia was observed with high carbohydrate intake. These results provide evidence for the rapid adaptation of the gut microbiota and host metabolism to high CHO in combination with 100% plant ingredients in rainbow trout.

To ensure the sustainability of aquaculture, it is necessary to change the “menu” of carnivorous fish such as rainbow trout from a fish-based diet to one with plant-based ingredients. However, there is a major problem with the growth performance decrease of fish fed with a 100% plant-based diet due to the reduction in feed intake and feed efficiency. For the first time, we incorporated high levels of digestible carbohydrates (high-starch diet) in a 100% plant-based diet during a 12-week feeding trial in order to improve protein utilization for growth (protein sparing effect) and reduce nitrogen waste. We measured the changes in the intestinal microbiota, Short-Chain Fatty Acid (SCFA) levels and metabolic responses in liver. Dietary carbohydrates had a strong effect on alpha and beta diversity and abundance of 12 genera, including Ralstonia and Bacillus in digesta associated microbiota whereas mucosa associated microbiota was less affected. The change in microbial diversity might be linked to the change observed in SCFA production. High levels of Mycoplasma were observed in the intestinal mucosa. Overall, hepatic gene expression was significantly altered by the CHO/protein ratio. Up-regulation of genes involved in glucose metabolism ( gcka , gckb , g6pcb2a ), down-regulation of genes involved in lipid metabolism ( hadh , acox3 , srebp2a , and cyp51a ) were associated with higher enzymatic activities (such as glucokinase or pyruvate kinase) and higher glycogen levels in the liver, suggesting adequate adaptation to diet. Interestingly, strong correlations were observed between abundances of certain bacterial OTUs and gene expression in the liver. The inclusion of digestible carbohydrates in combination with a 100% plant-based diet, could be a promising way to improve and reduce the use of plant proteins in rainbow trout. In addition, the relationship between intestinal microbiota and host metabolism needs further investigation to better understand fish nutrition.

Inulin affects nutrition and metabolism in many animals. Although inulin is widely used in the diet of teleosts, its mechanism of action is unknown. Here, we investigated the effect of inulin (2 %) on the intestinal microbiome and metabolism in rainbow trout ( Oncorhynchus mykiss ) selected for growth and survival when fed a 100 % plant-based diet ( suave ) and a control line ( temoin ). Metabolic responses to the two factors (line and inulin) in liver, intestine, muscle and adipose were tissue-specific, with line and interaction between the two factors influencing overall expression in liver. In the intestine, inulin and line and in muscle, line influenced the expression of metabolic genes. Microbiota between the mucus and digestive contents was significantly different, with genera from Proteobacteria being more abundant in the mucus, whereas genera from the Firmicutes and Planctomycetes being more abundant in contents. Effect of inulin and interaction between factors on the microbiome was evident in contents. The significant taxa of control and inulin-fed groups differed greatly with Streptococcus and Weissella being significantly abundant in the inulin-fed group. There was a general trend showing higher levels of all SCFA in temoin group with propionic acid levels being significantly higher. An operational taxonomic unit (OTU) belonging to the Ruminococcaceae was significantly abundant in suave . The tissue-specific correlations between OTU and gene expression may indicate the link between microbiome and metabolism. Together, these results suggest that line and inulin impact the gene expression in a tissue-specific manner, possibly driven by specific OTUs enriched in inulin-fed groups and suave .