Mushroom-based diets elicit region-specific shifts in rainbow trout gut microbiota

The intestinal microbiota of fish plays a crucial role in host condition and health, exhibiting region-specific functions influenced by dietary components. This study evaluated the effects of mushroom meals from Agaricus bisporus (AB), Lentinula edodes (LE), and Pleurotus ostreatus (PO) as alternative protein sources on the microbiota and histomorphology of the intestine in rainbow trout (Oncorhynchus mykiss). Experimental diets containing 30% of the above-mentioned mushroom meals were tested for 42 days under standard rearing conditions in rainbow trout juveniles weighting 120 g. At the end of the trial, mushroom meals did not affect the integrity of the intestinal mucosa while inducing a subtle region-specific shift in the intestinal microbial communities. These shifts were reflected in intra-individual (richness, Shannon, and Faith's phylogenetic diversity) and inter-individual diversity differences among diets (unweighted and weighted UniFrac distances). Specifically, Shannon index decreased in the pyloric caeca (PC), anterior (AI) and posterior intestine (PI) of fish fed the AB diet, while the observed richness and Faith's phylogenetic diversity showed a reduction in the AI and PI regions of fish fed the LE diet. Regarding composition, a consistent pattern found across the three intestinal regions was the high abundance of Desulfobacterota in fish fed the control diet (0% mushroom meals), which may be consequence of the higher content of dietary sulfur-containing amino acids, or due to unfavorable conditions resulting from fermentation of non-digestible polysaccharides from dietary plant protein sources. Regarding the mushroom-based diets, the AB diet promoted an increase in the abundance of potentially beneficial bacteria, such as Mycoplasma in the PC and AI, Legionella exclusively in the AI, and Weissella in the PI. In contrast, the PO diet increased the abundance of Paenibacillus in the PC, while the LE diet did not induce any relevant change in bacterial abundance at genus level. Additionally, the region-specific changes found in bacterial communities may reflect niche specialization and functional differentiation of the microbiota along the intestinal tract. In particular, the microbial changes of the PC seemed to be more associated to diet digestion and nutrient metabolism, while the AI might be related to the transient colonization of diet-derived bacteria. On the other hand, the PI microbiota was very conserved, and most likely linked to carbohydrate fermentation. Overall, these findings provide insights into the region-specific effects of functional dietary ingredients and highlight the potential use of mushroom meals as functional ingredients due to prebiotic effect as they beneficially modulate the intestinal microbiota and support intestinal health in rainbow trout.