Comparative metagenomics of tropical reef fishes show conserved core gut functions across hosts and diets with diet-related functional gene enrichments.

Abstract

Fish gut microbial communities are important for the breakdown and energy harvesting of the host diet. Microbes within the fish gut are selected by environmental and evolutionary factors. To understand how fish gut microbial communities are shaped by diet, three tropical fish species (hawkfish, Paracirrhites arcatus; yellow tang, Zebrasoma flavescens; and triggerfish, Rhinecanthus aculeatus) were fed piscivorous (fish meal pellets), herbivorous (seaweed), and invertivorous (shrimp) diets, respectively. From fecal samples, a total of 43 metagenome assembled genomes (MAGs) were recovered from all fish diet treatments. Each host-diet treatment harbored distinct microbial communities based on taxonomy, with Proteobacteria, Bacteroidota, and Firmicutes being the most represented. Based on their metagenomes, MAGs from all three host-diet treatments demonstrated a baseline ability to degrade proteinaceous, fatty acid, and simple carbohydrate inputs and carry out central carbon metabolism, lactate and formate fermentation, acetogenesis, nitrate respiration, and B vitamin synthesis. The herbivorous yellow tang harbored more functionally diverse MAGs with some complex polysaccharide degradation specialists, while the piscivorous hawkfish's MAGs were more specialized for the degradation of proteins. The invertivorous triggerfish's gut MAGs lacked many carbohydrate-degrading capabilities, resulting in them being more specialized and functionally uniform. Across all treatments, several MAGs were able to participate in only individual steps of the degradation of complex polysaccharides, suggestive of microbial community networks that degrade complex inputs.

Importance: The benefits of healthy microbiomes for vertebrate hosts include the breakdown of food into more readily usable forms and production of essential vitamins from their host's diet. Compositions of microbial communities in the guts of fish in response to diet have been studied, but there is a lack of a comprehensive understanding of the genome-based metabolic capabilities of specific microbes and how they support their hosts. Therefore, we assembled genomes of several gut microbes collected from the feces of three fish species that were being fed different diets to illustrate how individual microbes can carry out specific steps in the degradation and energy utilization of various food inputs and support their host. We found evidence that fish gut microbial communities share several core functions despite differences in microbial taxonomy. Herbivorous fish harbored a functionally diverse microbial community with plant matter degraders, while the piscivorous and invertivorous fish had microbiomes more specialized in protein degradation.