Genomic diversification of giant enteric symbionts reflects host dietary lifestyles

Herbivorous surgeonfishes are an ecologically successful group of reef fish that rely on marine algae as their principal food source. Here, we elucidated the significance of giant enteric symbionts colonizing these fishes regarding their roles in the digestive processes of hosts feeding predominantly on polysiphonous red algae and brown Turbinaria algae, which contain different polysaccharide constituents. Using metagenomics, single-cell genomics, and metatranscriptomic analyses, we provide evidence of metabolic diversification of enteric microbiota involved in the degradation of algal biomass in these fishes. The enteric microbiota is also phylogenetically and functionally simple relative to the complex lignocellulose-degrading microbiota of terrestrial herbivores. Over 90% of the enzymes for deconstructing algal polysaccharides emanate from members of a single bacterial lineage, "Candidatus Epulopiscium" and related giant bacteria. These symbionts lack cellulases but encode a distinctive and lineage-specific array of mostly intracellular carbohydrases concurrent with the unique and tractable dietary resources of their hosts. Importantly, enzymes initiating the breakdown of the abundant and complex algal polysaccharides also originate from these symbionts. These are also highly transcribed and peak according to the diel lifestyle of their host, further supporting their importance and host-symbiont cospeciation. Because of their distinctive genomic blueprint, we propose the classification of these giant bacteria into three candidate genera. Collectively, our findings show that the acquisition of metabolically distinct "Epulopiscium" symbionts in hosts feeding on compositionally varied algal diets is a key niche-partitioning driver in the nutritional ecology of herbivorous surgeonfishes.