Bacteria exist everywhere and readily adhere to natural and man-made solid surfaces such as soil, plants, animal tissue, teeth, medical implants, and pipelines. Some studies have shown that adhesion onto surfaces can affect the bacterial metabolic activity and survivability. While most of these studies focused on the availability of growth substrate at the surface, this study focuses on the direct affect of a surface on metabolic activity by examining a mechanistic link between the cellular bioenergetics and the physiochemical charge-regulation process. This is first known time that the potential link between these two processes has been studied.

The overall goal of this study was to determine the feasibility of this mechanistic link, and this was accomplished through a combination of experimental and numerical studies. The experimental studies focused on two bacterial species—Gram negative Escherichia coli and Gram positive Bacillus brevis. Experiments were conducted to (1) quantify the cell surface acid/base properties of these two species and (2) to examine how the presence of glass surfaces affects the bacterial metabolic activity, assessed through adenosine triphosphate (ATP) concentrations within the cells. First, through potentiometric titration experiments, it was shown that the charge-regulated bacterial surface has four distinct acid/base functional groups and that the distribution of these groups on the bacterial cell surface varied between E. coli and B. brevis. Second, through metabolic activity experiments, it was shown that bacterial adhesion onto a negatively charged glass surface resulted in a direct increase in bacterial ATP levels.

The data from these experiments was combined with numerical modeling to (i) calculate the bioenergetic proton-motive force (Δp) for adhered and planktonic bacteria, which directly drives ATP synthesis, and (ii) model the electrostatic behavior of the charge-regulated bacterial cell surface, with the purpose of determining if changes in electrostatic properties upon adhesion are sufficient to provide the changes in Δp identified in the first modeling effort. Proton-motive force calculations showed that Δp of the adhered bacteria was stimulated by increases in the pH gradient across the cell membrane. Charge-regulation modeling indicated that the proton concentration at the interface between a bacterium and the glass surface was two orders-of-magnitude greater than that of planktonic bacteria, and this was more than sufficient to provide the calculated increase in Δp and ultimately the observed increase in ATP levels.

The combined results of these numerical and experimental studies indicate that the link between the charge-regulation process and cellular bioenergetics is feasible. The results also indicate that the properties of the bacterial and solid surfaces must be considered together, as both impact bacterial metabolic activity. Ultimately, the knowledge gained in this study on the link between cellular bioenergetics and the charge-regulation effect will lead to further insight into bacterial interactions with other surfaces.