ABSTRACTDietary influence on the microbiome in algivorous sea urchins such asTripneustes gratilla elatensissuggests a bacterial contribution to the digestion of fiber-rich seaweed. An ecological insight into the spatial arrangement in the gut bacterial community will improve our knowledge of host-microbe relations concerning the involved taxa, their metabolic repertoire, and the niches of activity. Toward this goal, we investigated the bacterial communities in the esophagus, stomach, and intestine ofUlva-fed sea urchins through 16S rRNA amplicon sequencing, followed by the prediction of their functional genes. We revealed communities with distinct features, especially those in the esophagus and intestine. The esophageal community was less diverse and was poor in food digestive or fermentation genes. In contrast, bacteria that can contribute to the digestion of the dietaryUlvawere common in the stomach and intestine and consisted of genes for carbohydrate decomposition, fermentation, synthesis of short-chain fatty acids, and various ways of N and S metabolism.BacteroidetesandFirmicuteswere found as the main phyla in the gut and are presumably also necessary in food digestion. The abundant sulfate-reducing bacteria in the stomach and intestine from the generaDesulfotalea,Desulfitispora, andDefluviitaleamay aid in removing the excess sulfate from the decomposition of the algal polysaccharides. Although these sea urchins were fed withUlva, genes for the degradation of polysaccharides of other algae and plants were present in this sea urchin gut microbiome. We conclude that the succession of microbial communities along the gut obtained supports the hypothesis on bacterial contribution to food digestion.IMPORTANCEAlga grazing by the sea urchinTripneustes gratilla elatensisis vital for nutrient recycling and constructing new reefs. This research was driven by the need to expand the knowledge of bacteria that may aid this host in alga digestion and their phylogeny, roles, and activity niches. We hypothesized alterations in the bacterial compositional structure along the gut and their association with the potential contribution to food digestion. The current spatial insight into the sea urchin’s gut microbiome ecology is novel and reveals how distinct bacterial communities are when distant from each other in this organ. It points to keynote bacteria with genes that may aid the host in the digestion of the complex sulfated polysaccharides in dietaryUlvaby removing the released sulfates and fermentation to provide energy. The gut bacteria’s genomic arsenal may also help to gain energy from diets of other algae and plants.