Ruminococcus bromii enables the growth of proximal Bacteroides thetaiotaomicron by releasing glucose during starch degradation

Authors:
Preprint
Publisher website
Google Scholar
Abstract
Complex carbohydrates shape the gut microbiota and the collective fermentation of resistant starch by gut microbes positively affects human health through enhanced butyrate production. The keystone species Ruminococcus bromii ( Rb ) is a specialist in degrading resistant starch; its degradation products are used by other bacteria including Bacteroides thetaiotaomicron ( Bt ). We analyzed the metabolic and spatial relationships between Rb and Bt during potato starch degradation and found that Bt utilizes glucose that is released from Rb upon degradation of resistant potato starch and soluble potato amylopectin. Additionally, we found that Rb produces a halo of glucose around it when grown on solid media containing potato amylopectin and that Bt cells deficient for growth on potato amylopectin (Δ sus Bt ) can grow within the halo. Furthermore, when these Δ sus Bt cells grow within this glucose halo, they have an elongated cell morphology. This long-cell phenotype depends on the glucose concentration in the solid media: longer Bt cells are formed at higher glucose concentrations. Together, our results indicate that starch degradation by Rb cross-feeds other bacteria in the surrounding region by releasing glucose. Our results also elucidate the adaptive morphology of Bt cells under different nutrient and physiological conditions. Impact Statement: Dietary intake of complex carbohydrates including resistant starch benefits human health by supporting the growth of keystone species that increase the microbiome diversity via cross-feeding. For instance, Ruminococcus bromii ( Rb ) is a specialist in degrading resistant starch, and the byproducts of this degradation process are used by bacterial species. In this study, we show that Bacteroides thetaiotaomicron ( Bt ) cross-feeds on the glucose released during potato starch degradation by Rb . We also show that proximity to Rb cells that are releasing sugars is important for the growth of the cross-fed Bt in solid media. Additionally, we find a longer phenotype for Bt cells grown on solid media in high glucose conditions, indicating that, like other bacteria, human gut bacteria undergo significant nutrient-dependent morphological adaptations.
All Related Versions

This publication has 54 references indexed in Scilit: