Selection for non-specific adhesion is a driver of FimH evolution increasing Escherichia coli biofilm capacities

Bacterial interactions with surfaces and the subsequent formation of biofilms essentially rely on their ability to timely express, assemble and expose various adhesion factors. Whereas a coordinated interplay between proteinaceous adhesins or macromolecular exopolymers are required for successful bacterial colonization, how bacteria dynamically modulates their surface-binding potential is not yet well understood. We investigated the modification of the biofilm capacity of an initially poorly adherent Escherichia coli strain using experimental evolution and positive selection for mutations improving biofilm formation. We showed that, despite its vast adhesion repertoire, all evolved clones with increased biofilm-forming capacity corresponded to mutations located in fimH, the gene coding for the a-D-mannose-specific tip adhesin of type 1 fimbriae. While most of these mutants showed reduced mannose-binding ability, they all displayed enhanced non-specific surface binding and outcompeted comparatively more fragile biofilm-forming mutants obtained by positive selection performed in a delta-fim background. Moreover, we showed that several of the fimH mutations identified in our study corresponded to mutations found in pathogenic and environmental E. coli, suggesting that fimH microevolution favoring biofilm capacity could constitute a selective advantage for clinical or natural E. coli isolates. Beyond providing direct insights into the plasticity of E. coli adhesion potential, our study showed that selection for non-specific adhesion drives FimH evolution and extends its mutational landscape beyond patho-adaptation, suggesting a host versus environment trade-off between FimH-mediated specific and non-specific adhesion properties.