Fluid flow structures gut microbiota biofilm communities by distributing public goods

Bacterial gut commensals experience a biologically and physically complex mucosal environment. While many chemical factors mediate the composition and structure of these microbial communities, less is known about the role of mechanics. Here, we demonstrate that fluid flow impacts the spatial organization and composition of gut biofilm communities by shaping how different species interact metabolically. We first demonstrate that a model community composed of Bacteroides thetaiotaomicron (Bt) and Bacteroides fragilis (Bf), two representative human commensals, can form robust biofilms in flow. We identified dextran as a polysaccharide readily metabolized by Bt but not Bf, but whose fermentation generates a public good enabling Bf growth. By combining simulations with experiments, we demonstrate that in flow, Btbiofilms share dextran metabolic by-products, promoting Bf biofilm formation. By transporting this public good, flow structures the spatial organization of the community, positioning the Bf population downstream from Bt. We show that sufficiently strong flows abolish Bf biofilm formation by limiting the effective public good concentration at the surface. Physical factors such as flow may therefore contribute to the composition of intestinal microbial communities, potentially impacting host health.

Automated summary

Bacterial gut commensals are affected by the complex mucosal environment, and the role of mechanics, including fluid flow, in shaping microbial communities is not well understood. This study demonstrates that fluid flow influences the spatial organization and composition of gut biofilm communities by affecting species interactions and metabolic processes. In particular, the transport of a metabolic by-product, dextran, promotes the formation of biofilms composed of Bacteroides fragilis downstream from Bacteroides thetaiotaomicron. Strong flows, however, can limit the formation of B. fragilis biofilms by reducing the concentration of this public good. These findings suggest that physical factors like flow may play a role in shaping intestinal microbial communities and potentially impacting host health.