Bacterial adhesion to and subsequent colonization of surfaces are the first steps toward forming biofilms, which are a major concern for implanted medical devices and in many diseases. It has generally been assumed that strong irreversible adhesion is a necessary step for biofilm formation. However, some bacteria, such as Escherichia coli when binding to mannosylated surfaces via the adhesive protein FimH, adhere weakly in a mode that allows them to roll across the surface. Since single-point mutations or even increased shear stress can switch this FimH-mediated adhesion to a strong stationary mode, the FimH system offers a unique opportunity to investigate the role of the strength of adhesion independently from the many other factors that may affect surface colonization. Here we compare levels of surface colonization by E. coli strains that differ in the strength of adhesion as a result of flow conditions or point mutations in FimH. We show that the weak rolling mode of surface adhesion can allow a more rapid spreading during growth on a surface in the presence of fluid flow. Indeed, an attempt to inhibit the adhesion of strongly adherent bacteria by blocking mannose receptors with a soluble inhibitor actually increased the rate of surface colonization by allowing the bacteria to roll. This work suggests that (i) a physiological advantage to the weak adhesion demonstrated by commensal variants of FimH bacteria may be to allow rapid surface colonization and (ii) antiadhesive therapies intended to prevent biofilm formation can have the unintended effect of enhancing the rate of surface colonization.Biofilms consist of surface-associated colonies of bacteria (11, 45) and are a major concern for implanted medical devices and in many diseases. They are the dominant mode of bacterial life in nature and exist on biological as well as abiotic surfaces (11,45). Eradication of biofilms is more problematic than that of bacteria in the planktonic mode of growth, since biofilms are resistant to innate host defenses (21, 32, 51), mechanical removal, and antibiotic treatments (6, 52). Therefore, a more promising strategy that has been proposed is to prevent biofilm formation through interference with the earliest steps of formation (11,38,45). Surface adhesion, defined as the binding of a planktonic bacterium to a surface, is the first step, and it is generally assumed that strong irreversible adhesion is necessary for biofilm formation (9,14). The next step is surface colonization, defined as the spread of adherent bacteria across a surface through division. It has been suggested that biofilms can be prevented by restricting these early stages of colonization by blocking specific receptor-ligand interactions with soluble inhibitors or antibodies that block adhesion rather than prevent bacterial growth (39).Escherichia coli binding via the protein FimH provides a model system for studying surface adhesion and colonization for two reasons. First, E. coli is the most common cause of both urinary tract infections (22, 23) and bi...
Shear-enhanced adhesion, although not observed for fimbria-mediated adhesion of oral Actinomyces spp., was noted for Hsa-mediated adhesion of Streptococcus gordonii to sialic acid-containing receptors, an interaction implicated in the pathogenesis of infective endocarditis.Colonization of the tooth surface involves adhesin-mediated interactions between different species of bacteria and between bacteria and salivary components adsorbed onto the acquired enamel pellicle (11,16). Examples include Hsa-mediated attachment of Streptococcus gordonii to ␣2-3-linked sialic acid termini of mucinous glycoproteins (18,21,23), type 1 fimbriamediated attachment of Actinomyces oris (formerly Actinomyces naeslundii) to proline-rich proteins (PRPs) (9, 15), and type 2 fimbria-mediated attachment of A. oris and of A. naeslundii to Gal1-3GalNAc motifs in mucins (15). Type 2 fimbriae also recognize Gal1-3GalNAc motifs in cell surface receptor polysaccharides (RPS) of certain initial colonizing streptococci (4). Importantly, all these interactions occur in the presence of soluble salivary components that are potential inhibitors of adhesion. Thus, to fulfill their biological role, the corresponding adhesins must be selective for surface-associated receptor molecules rather than for their soluble counterparts. For example, type 1 fimbria-mediated adhesion of actinomyces to surface-associated PRP is not inhibited by soluble PRP (8); exposure of a cryptic receptor on PRP molecules upon adsorption to the tooth surface was postulated. A different mechanism was suggested for type 2 fimbria-mediated adhesion of Actinomyces spp. in the presence of soluble mucins. In this case, heavily fimbriated cells were thought to bind with greater avidity to surface-associated receptors (5).Another explanation for bacterial adhesion in the presence of soluble receptors has emerged from recent studies on the effect of shear force on fimbria-mediated adhesion of Escherichia coli to mannose-containing receptors (17,24,25). At low shear, cells attached weakly and rolled along the receptorcoated substratum. As shear was increased, cells became stationary; subsequent reduction in shear caused the cells to resume rolling. These reversible changes in adhesion strength were postulated to arise from shear-dependent drag force on bacteria when bound to surface-associated ligands. Structural data suggested that a shear-dependent conformational change in the mannose-binding fimbrial adhesin FimH resulted from the formation of a so-called catch bond that increased the strength of the adhesin-ligand interaction. This increase may favor recognition of surface-associated receptors over soluble receptors because soluble receptors are not subject to shear stress and thus cannot induce catch bond formation.Examples of shear-enhanced adhesion also include the interaction between von Willebrand factor and GPIb␣ on platelets (7) and recognition of P-selectin by P-selectin glycoprotein ligand on leukocytes (12). The present study addresses whether fimbria-mediated adhesion o...
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