Abstract

Prediction of individualized responses is one of biggest challenges in dietary intervention to modulate human gut microbiota. Bacterial interspecies competition for dietary factors should underlie the inter-subject heterogeneity of microbial responses. Microscale localization of bacterial species around intestinal food structures could provide direct evidence for understanding this, however, little information is currently available. Here we analyzed human fecal sections and found multiple types of bacterial colonization of food structures. The most eminent one was dense and frequent colonization of starch granules by Bifidobacterium adolescentis. After intake of raw potato starch (pSt), B. adolescentis dramatically increased in every carrier of the species, accompanied by an increase in bifidobacterial metabolite acetate. In the other subjects, Eubacterium rectale and its metabolite butyrate increased, but it was suppressed in B. adolescentis carriers. A correlation analysis indicated the contribution of these species to respective metabolites. In vitro analyses of isolates of major gut bacterial species confirmed that these species are major colonizers of pSt and that B. adolescentis can colonize pSt even in the presence of the known starch granule–degrading bacterium Ruminococcus bromii. Collectively, we propose that specific binding of B. adolescentis or E. rectale to pSt selectively induces acetogenic or butyrogenic response of gut microbiota, where the former determines the response of the latter.

Highlights

  • The intestinal microbiota contributes to many aspects of host health and diseases via bioactive metabolites including shortchain fatty acids (SCFAs)

  • Stool samples were collected from five subjects who were taking habitual diet, and fecal paraffin sections were analyzed by fluorescence in situ hybridization (FISH) with probes specific for major bacterial taxa

  • For B. adolescentis, positive correlation was found with B. longum and Collinsella aerofaciens. These results strongly suggest that (i) among all bacterial species detected in this study, B. adolescentis most efficiently consumes intestinal potato starch (pSt) granules, which is facilitated by their colonization, to increase its abundance and generation of acetic and lactic acids, and that (ii) E. rectale can increase its abundance upon pSt intake, generating butyrate, but only in the absence of the dominant consumer B. adolescentis

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Summary

Introduction

The intestinal microbiota contributes to many aspects of host health and diseases via bioactive metabolites including shortchain fatty acids (SCFAs). A specific set of gut bacteria expands upon taking up each food, including indigestible polysaccharides, in some cases after degradation by host or microbial enzymes [4,5,6,7]. Direct utilization of each nutrient in the intestine by specific human gut–associated bacteria has been demonstrated using isolated strains and recently predicted from genomic data. A recent study showed a conceptual example of interspecies competition for a nutrient by using gnotobiotic mice [8], competitions and key behaviors are largely unidentified in vivo or in situ by analyzing normal human intestinal microbiota. We show specific bacterial colonization of a specific type of starch in human fecal sections, and show the impact of the major colonizing species on the response of microbiota to a nutrient that is competed for by multiple gut bacterial species. The major gut fermentation product in each subject was determined by which of the two species responded and especially by the presence of B. adolescentis

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