Adhesion of E. coli bacteria is force-modulated due to fimbriae-mediated surface repulsion and multivalent binding irrespective of surface specificity

Abstract

Escherichia coli bacteria that express type 1 fimbriae migrate along surfaces when pushed by a slow flow but stick more firmly when the flow increases. This and other examples of force-modulated biological binding are often described as due to lectin-glycan catch-bonds. Here we quantitatively track the 3D movements of fimbriated E. coli flowing over surfaces nanopatterned with mannose or hydrophobic binding sites. We reveal that flow-modulated surface adhesion and motion are consequences of bacteria adhering via polydisperse, elastic fimbriae, irrespective of binding affinity and specificity. The fimbria-mediated surface repulsion and the flow forces on tethered bacteria establish an equilibrium bacteria-surface separation. The separation controls the number of potential tethers between the bacterium and the surface. Combined with the individual fimbria affinity, this determines the surface avidity and surface motion. This provides a broadly applicable mechanism by which bacteria acquire adaptive surface avidity, responding super-selectively to different flow environments, concentration, and affinity of available binding sites, essential to explaining how fimbriae govern tropism and surface colonization.