Variation in Bacterial ATP Level and Proton Motive Force Due to Adhesion to a Solid Surface

Abstract

Bacterial adhesion to natural and man-made surfaces can be beneficial or detrimental, depending on the system at hand. Of vital importance is how the process of adhesion affects the bacterial metabolic activity. If activity is enhanced, this may help the cells colonize the surface, whereas if activity is reduced, it may inhibit colonization. Here, we report a study demonstrating that adhesion of both Escherichia coli and Bacillus brevis onto a glass surface resulted in enhanced metabolic activity, assessed through ATP measurements. Specifically, ATP levels were found to increase two to five times upon adhesion compared to ATP levels in corresponding planktonic cells. To explain this effect on ATP levels, we propose the hypothesis that bacteria can take advantage of a link between cellular bioenergetics (proton motive force and ATP formation) and the physiochemical charge regulation effect, which occurs as a surface containing ionizable functional groups (e.g., the bacterial cell surface) approaches another surface. As the bacterium approaches the surface, the charge regulation effect causes the charge and pH at the cell surface to vary as a function of separation distance. With negatively charged surfaces, this results in a decrease in pH at the cell surface, which enhances the proton motive force and ATP concentration. Calculations demonstrated that a change in pH across the cell membrane of only 0.2 to 0.5 units is sufficient to achieve the observed ATP increases. Similarly, the hypothesis indicates that positively charged surfaces will decrease metabolic activity, and results from studies of positively charged surfaces support this finding.