Fluid flow structures gut microbiota biofilm communities by distributing public goods

Author:

Wong Jeremy P. H.12ORCID,Fischer-Stettler Michaela3,Zeeman Samuel C.3ORCID,Battin Tom J.2,Persat Alexandre1ORCID

Affiliation:

1. Institute of Bioengineering and Global Health Institute, School of Life Sciences, École Polytechnique Fédérale de Lausanne, Lausanne 1015, Switzerland

2. School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne, Lausanne 1015, Switzerland

3. Department of Biology, ETH Zürich, Zürich 8092, Switzerland

Abstract

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, Bt biofilms 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.

Funder

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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