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Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish.

ABSTRACT: Many marine herbivorous fishes harbour diverse microbial communities in the hindgut that can play important roles in host health and nutrition. Kyphosus sydneyanus is a temperate marine herbivorous fish that feeds predominantly on brown seaweeds. We employed 16S rRNA gene amplicon sequencing and gas chromatography to characterize microbial communities and their metabolites in different hindgut regions of six K. sydneyanus. Measurements were confined to three distal sections of the intestine, labelled III, IV and V from anterior to posterior. A total of 625 operational taxonomic units from 20 phyla and 123 genera were obtained. Bacteroidota, Firmicutes and Proteobacteria were the major phyla in mean relative abundance, which varied along the gut. Firmicutes (76%) was the most dominant group in section III, whereas Bacteroidota (69.3%) dominated section V. Total short-chain fatty acid (SCFA) concentration was highest in sections IV and V, confirming active fermentation in these two most distal sections. The abundance of Bacteroidota correlated with propionate concentration in section V, while Firmicutes positively correlated with formate in sections III and IV. Acetate levels were highest in sections IV and V, which correlated with abundance of Bacteroidota. Despite differences in gut microbial community composition, SCFA profiles were consistent between individual fish in the different hindgut regions of K. sydneyanus, although proportions of SCFAs differed among gut sections. These findings demonstrate functional compartmentalization of the hindgut microbial community, highlighting the need for regional sampling when interpreting overall microbiome function. These results support previous work suggesting that hindgut microbiota in marine herbivorous fish are important to nutrition in some host species by converting dietary carbohydrates into metabolically useful SCFAs.

SUBMITTER: Pardesi B

PROVIDER: S-EPMC9306998 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundGut microbiota play a key role in the nutrition of many marine herbivorous fishes through hindgut fermentation of seaweed. Gut microbiota composition in the herbivorous fish Kyphosus sydneyanus (family Kyphosidae) varies between individuals and gut sections, raising two questions: (i) is community composition stable over time, especially given seasonal shifts in storage metabolites of dietary brown algae, and (ii) what processes influence community assembly in the hindgut?ResultsWe examined variation in community composition in gut lumen and mucosa samples from three hindgut sections of K. sydneyanus collected at various time points in 2020 and 2021 from reefs near Great Barrier Island, New Zealand. 16S rRNA gene analysis was used to characterize microbial community composition, diversity and estimated density. Differences in community composition between gut sections remained relatively stable over time, with little evidence of temporal variation. Clostridia dominated the proximal hindgut sections and Bacteroidia the most distal section. Differences were detected in microbial composition between lumen and mucosa, especially at genus level.ConclusionsHigh variation in community composition and estimated bacterial density among individual fish combined with low variation in community composition temporally suggests that initial community assembly involved environmental selection and random sampling/neutral effects. Community stability following colonisation could also be influenced by historical contingency, where early colonizing members of the community may have a selective advantage. The impact of temporal changes in the algae may be limited by the dynamics of substrate depletion along the gut following feeding, i.e. the depletion of storage metabolites in the proximal hindgut. Estimated bacterial density, showed that Bacteroidota has the highest density (copies/mL) in distal-most lumen section V, where SCFA concentrations are highest. Bacteroidota genera Alistipes and Rikenella may play important roles in the breakdown of seaweed into useful compounds for the fish host.

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Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish.

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