Prebiotics modify host metabolism in rainbow trout (Oncorhynchus mykiss) fed with a total plant-based diet: Potential implications for microbiome-mediated diet optimization

The use of plant-based ingredients in aquafeeds is increasing because marine sources of protein and oil are unsustainable. However, plant-based ingredients cause certain metabolic complications in carnivorous species such as rainbow trout. Here, we examined whether prebiotics have the potential to affect the metabolism of juvenile trout (Average weight: 25.88 ± 0.91 g) via microbially derived short-chain fatty acids (SCFAs). Fructo-oligosaccharides (FOS), inulin or mannan-oligosaccharides (MOS) were used at 1% or 2% in a 12-week feeding experiment. We measured changes in the intestinal microbiome, SCFA levels and metabolic responses in the intestine, liver, muscle, and adipose tissue. In the intestine, gene expression and SCFA production did not change significantly with prebiotics, although the MOS fed groups were clustered differently. Prebiotics had a significant effect on the intestinal abundance of Bacillus, Lactobacillus and Weissella in a dose dependent manner, although the microbial diversity (alpha and beta) did not change significantly after feeding prebiotics. Two operational taxonomic units (OTUs) belonging to the genus Mycoplasma dominated all samples with an average relative abundance of >95% per group. Intestinal microvillar structures were significantly improved in length in the inulin-fed groups. Systemically, overall hepatic gene expression was significantly different from control with inulin-fed groups showing upregulation of several metabolic and the fatty acid receptor genes. MOS fed groups showed a dose-dependent but contrasting response in liver and muscle. In addition, a significant effect of prebiotic and the interaction between the 2 factors (prebiotic and dose) on final weight and SGR respectively, was observed. The relative abundance of OTUs belonging to Lactobacillus and Bacillus correlated with hepatic gene expression and final weight of the fish. Inulin and MOS appear to differentially affect host metabolism, mainly in the liver and muscle. Differential abundance of Lactobacillus and Bacillus in the prebiotic-fed groups and their correlations with hepatic gene expression could indicate a prebiotic-microbiome-host axis, although this was not conclusively shown through the levels of SCFAs. In combination with a total plant-based diet, inulin could be a promising prebiotic for trout but need to be further investigated. These findings could implicate in microbiome-mediated dietary optimization of rainbow trout.