Genomic diversification of giant enteric symbionts reflects host dietary lifestyles

Abstract

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.piscine herbivores | marine algae | carbohydrases | giant enteric symbionts | Epulopiscium M arine herbivorous fishes are an ecologically dominant force, structuring tropical reef ecosystem functions and relationships through their grazing activities (1-3). However, they are one of the least understood guilds of herbivores regarding the mechanisms by which they digest and assimilate algal biomass, especially in contrast to plant material assimilation by terrestrial vertebrate herbivores and insects (1, 4). In terrestrial herbivores, the community of microbes inhabiting an organism's gut-the gut microbiota-is considered to play a significant role in the organism's ability to digest plant matter. It is thought to be a major factor leading to the evolution of vertebrate and insect-based herbivory (1-3, 5) and constitutes a potentially critical component of diet-driven speciation in mammals (1,4,6). Contrary to the immense literature on the nutritional ecology and plant biomass assimilation by mammals, ruminants, and arthropods (4,7,8), mechanistic insights into the digestive physiology of marine herbivores, especially the roles of gastrointestinal microbes of piscine herbivores in gut digestive processes, remain largely uncharacteriz...

Intestinal microbes: an axis of functional diversity among large marine consumers

“…However, their putative functions in the intestine are unclear. Metagenomic analyses and studies that experimentally elucidate the functions of intestinal microbes [41] are particularly needed to disentangle which microbiome members are drivers versus passengers of herbivorous fish feeding behaviour.…”

Extensive transfer of genes for edible seaweed digestion from marine to human gut bacteria

“…( Fig. 5C , Extended Data 9, Supplemental Tables 11, 12, 13 ), the latter being abundant colonizers of marine surgeonfish 27 . Sequence-based surveys of surgeonfish gut microbiomes have previously detected enzymes in these same families in metagenome- and single cell isolation-based genome sequences belonging to Epulopiscium spp.…”

Feeding behavior in Caribbean surgeonfishes varies across fish size, algal abundance, and habitat characteristics

“…Other surgeonfishes with different diets such as Ctenochaetus striatus (bristle-like teeth) and A. nigrofuscus (incisiform teeth) display very different dental morphology (Tebbett et al, 2017a). It is quite possible that the two species in our study are partitioning the turf community along axes that we did not resolve here, and thus, further studies such as analysis of composition of the their gastrointestinal symbionts (Ngugi et al, 2017) may help to elucidate differences in their feeding niches.…”

“…By contrast, as a result of less efficient methods of processing its food, higher gut turnover rates could be required by A. tractus , akin to terrestrial hindgut fermenters. Other factors such as the enzymatic activity carried out by endosymbiotic bacteria (Ngugi et al, ) might also influence the digestive capabilities of Caribbean Acanthurus species but further work is needed to test this hypothesis.…”