Anatomical site and environmental exposure differentially shape the microbiota acorss mucosal tissues in rainbow trout (Oncorhynchus mykiss)

Abstract

This study investigates the diversity, structure, and composition of the fish microbiota across different mucosal organs by comparing the bacterial communities in the oropharyngeal cavity, posterior intestine, gills, and skin of farmed rainbow trout (Oncorhynchus mykiss), along with water and biofilm samples from the surrounding environment. Four distinct skin regions across the dorsal-ventral and anterior-posterior axes were also compared in fish weighing 390.5 ± 36.8 g. Sample analyses showed that lower values of richness (observed) and diversity (Shannon and Faith indices) were observed in the posterior intestine compared to the gills, skin, and environmental (water and biofilm) samples (P < 0.05). Similarly, the oropharynx showed higher Faith diversity values than the intestine (P = 0.01). Furthermore, bacterial community structures differed significantly across organs based on unweighted and weighted UniFrac distances (P = 0.001 for both), with the posterior intestine showing the greatest divergence from other mucosal sites. Indeed, Pseudomonadota was the most abundant phylum across all sample types, except for the posterior intestine, where Firmicutes, particularly the genus Mycoplasma, showed a clear predominance. The posterior intestine showed facultative anaerobic genera, while the other mucosae and environmental samples were mainly composed of strictly aerobic members, like Flavobacterium and Crocinitomix. The microbial communities across the different skin regions were highly heterogeneous: while the dorsal area showed a consistent microbiota, the ventral region exhibited differences between the anterior and posterior sections in bacterial structure and composition at the genus level (P < 0.05). For instance, Candidatus Piscichlamydia was very abundant in the gills and ventral-anterior skin, but was scarcely detected in the rest of skin areas. Overall, these findings suggest a high differentiation of bacterial communities across fish organs, tailored to the specific physiological and environmental characteristics of each mucosal tissue, with a stronger modulation by the surrounding environment in the external mucosae and a higher influence of host innate factors in inner organs, such as the intestine.