Abstract
The development of bacteria on abiotic surfaces has important public health and sanitary consequences. However, despite several decades of study of bacterial adhesion to inert surfaces, the biophysical mechanisms governing this process remain poorly understood, due, in particular, to the lack of methodologies covering the appropriate time scale. Using micrometric colloidal surface particles and flow cytometry analysis, we developed a rapid multiparametric approach to studying early events in adhesion of the bacterium Escherichia coli. This approach simultaneously describes the kinetics and amplitude of early steps in adhesion, changes in physicochemical surface properties within the first few seconds of adhesion, and the self-association state of attached and free-floating cells. Examination of the role of three well-characterized E. coli surface adhesion factors upon attachment to colloidal surfaces—curli fimbriae, F-conjugative pilus, and Ag43 adhesin—showed clear-cut differences in the very initial phases of surface colonization for cell-bearing surface structures, all known to promote biofilm development. Our multiparametric analysis revealed a correlation in the adhesion phase with cell-to-cell aggregation properties and demonstrated that this phenomenon amplified surface colonization once initial cell-surface attachment was achieved. Monitoring of real-time physico-chemical particle surface properties showed that surface-active molecules of bacterial origin quickly modified surface properties, providing new insight into the intricate relations connecting abiotic surface physicochemical properties and bacterial adhesion. Hence, the biophysical analytical method described here provides a new and relevant approach to quantitatively and kinetically investigating bacterial adhesion and biofilm development.
Highlights
Bacterial growth on surfaces and interfaces leads to the formation of three-dimensional communities called biofilms [1]
We introduced an original approach to investigating the very early steps in bacterial adhesion that uses dispersed colloidal surfaces as microbial adhesion substrates
We demonstrate that initial adhesion correlates with almost instant surface property changes, and that cell-to-cell association might serve as an amplification mechanism for surface colonization
Summary
Bacterial growth on surfaces and interfaces leads to the formation of three-dimensional communities called biofilms [1]. Physico-chemical approaches based on the DerjaguinLandau-Verwey-Overbeek (DLVO) [4] theory, reliable in predicting interactions between well-controlled model hard spheres, have often proven inappropriate for modeling bacterial adhesion [5]. This is likely due to the multiplicity of parameters involved in the adhesion process, influenced both by biological and environmental factors. Interpretations are often made at the final adsorption stage or at equilibrium, when initial adhesion is blurred by subsequent biofilm development steps, preventing precise kinetic analysis of the adhesion process [3]. Alternative short-term approaches are needed to provide quantitative and kinetic information on the early stage of bacterial interaction with a surface
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