Selective induction of human gut-associated acetogenic/butyrogenic microbiota based on specific microbial colonization of indigestible starch granules

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.