Diet-Induced Shifts in the Hindgut Microbiome Leads to Subtle Changes in Gut and Liver Function of a Marine Herbivorous Fish

AbstractThe diet of an organism can influence various biological processes, including digestion. By examining how dietary changes can shift gut physiology in an herbivorous fish, we can gain insight into what that species can tolerate in terms of dietary shifts. Thus, we investigated how gut mass, digestive enzyme activity, hindgut microbial diversity, levels of gastrointestinal fermentation, and hindgut and liver transcriptomics respond to dietary perturbations in the marine herbivorous fish Cebidichthys violaceus. Contrary to our expectations, fish fed an omnivore diet (45% protein) in the laboratory exhibited the most similarity to wild-caught herbivorous fish, sharing a high abundance of taxa in the Bacteroidota and Bacillota phyla (families Ruminococcaceae and Rikenellaceae) and the highest concentrations of short-chain fatty acids. Fish in these groups shared similarities in gene expression patterns too. Fish fed herbivore (~23% protein) or carnivore (~69% protein) diets in the laboratory had a high abundance of taxa from the Pseudomonadota phylum (families Burkholderiaceae and Oxalobacteraceae) and lower short-chain fatty acid concentrations. The hindgut had 519 differentially expressed genes, with wild-caught fish exhibiting a high expression of genes associated with ion transport, lipid metabolism, and glucose metabolism. The liver had 4,650 differentially expressed genes, and wild-caught fish had a high expression of genes related to fatty acid synthesis and proteolysis. Hindgut digestive enzyme activities also varied with diet and microbial diversity. Our integrative study furthers our understanding of the physiology of an herbivorous fish and how it responds to shifting dietary resources, particularly with an eye toward herbivorous fish aquaculture.