Weak Rolling Adhesion Enhances Bacterial Surface Colonization

Abstract

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...

Differential Stability and Trade-Off Effects of Pathoadaptive Mutations in the Escherichia coli FimH Adhesin

“…It also might prove to be a significant disadvantage in other compartments critical for populational stability of E. coli, where the shear level is relatively high. For example, recently it has been shown that strong and firm 1M binding inhibits the spread of developing E. coli biofilms under flow conditions (1).…”

Adaptive mutations in the signal peptide of the type 1 fimbrial adhesin of uropathogenic Escherichia coli

“…Although the details of the conformational link between the interdomain configuration and the binding site are unclear, the allosteric properties of FimH are strongly supported by the presence in FimH of an integrin-like ligand-induced binding site epitope for monoclonal antibodies and by single-molecule studies using AFM (28). This catch bond mechanism was shown to provide a means for resistance of bacterial adhesion to soluble inhibitors and for surface spreading in biofilm formation (29).…”

Antibacterial Effect of Ethanolic Extract of Allium sativum on Biofilm Forming Staphylococcus aureus which Cause Folliculitis

“…Bacterial adhesion and subsequent colonization of surfaces are the first step toward biofilm formation. Biofilm consisted of microcolonies encased in extracellular polysaccharide material which formed under selected conditions (Olson et al, 2002;Anderson et al, 2007). The biofilm develops on both living surfaces and artificial implants which allow the bacteria to persist for long period by establishment of dormant reservoir of pathogens, re-emergence of bacteria from this reservoir might be the source of recurrent infection (Deleo et al, 2010).…”