Effects of a low-lipid diet on the gut microbiome and head kidney transcriptome of juvenile Chinook Salmon

Abstract

Objective Pacific salmon Oncorhynchus spp. reared in production hatcheries are typically fed high-lipid, energy-dense diets to achieve large size and high body condition prior to release. In contrast, juveniles in natural environments tend to consume low-lipid, high-protein diets, and fish reared for research or conservation purposes are sometimes fed diets that are formulated to mimic natural diets and promote wild-like phenotypes. Understanding how these alternative diets affect fish health beyond growth and body condition could ultimately contribute to improving hatchery fish fitness. Methods In this work, we evaluated changes in the fecal microbiome and gene expression of juvenile Chinook Salmon O. tshawytscha on a standard high-lipid hatchery diet versus a low-lipid diet formulated to mimic the nutrition profile of natural-origin fish. To evaluate the time scale at which diet alters the fecal microbiome, we collected longitudinal samples over a 12-week period and switched the diets of a subset of fish twice during the experiment. We used 16S ribosomal RNA gene amplicon sequencing to characterize fecal microbiome differences between fish on the two diets as well as hatchery-reared fish at a production hatchery, hatchery fish that had been captured after release into a stream, and natural-origin, stream-reared fish of similar ages. Additionally, we conducted RNA sequencing on head kidney samples from laboratory-reared fish to evaluate changes in gene expression in this important immune organ. Results We found that the low-lipid diet and the hatchery diet resulted in microbiomes that differed from the microbiome of natural-origin fish and from each other and that diet-driven changes to the microbiome could occur in under 14 d. The low-lipid diet did not result in a microbiome that resembled the microbiome of naturally produced fish. Instead, the low-lipid diet resulted in a microbiome community that was distinct from those of fish reared on the hatchery diet and fish sampled from the wild. The RNA sequencing results indicated differential enrichment of pathways related to immunity, metabolism, and hormone synthesis between fish that were fed the two experimental diets. Conclusions The results suggest that additional environmental factors influence the microbiome more strongly than diet formulation or that the low-lipid diet has a smaller effect on the microbiome than a natural, ­invertebrate-based diet. Given that the gut microbiome and systemic immune function contribute significantly to disease resistance, our findings highlight the importance of understanding how diets fed to fish in captivity may affect fish health beyond growth and body condition metrics.