Alteration of bacterial surface electrostatic potential and pH upon adhesion to a solid surface and impacts to cellular bioenergetics

Abstract

In our previous study [Hong Y, Brown DG (2009) Appl Environ Microbiol 75(8):2346-2353], the adenosine triphosphate (ATP) level of adhered bacteria was observed to be 2-5 times higher than that of planktonic bacteria. Consequently, the proton motive force (Delta p) of adhered bacteria was approximately 15% greater than that of planktonic bacteria. It was hypothesized that the cell surface pH changes upon adhesion due to the charge-regulated nature of the bacterial cell surface and that this change in surface pH can propagate to the cytoplasmic membrane and alter Delta p. In the current study, we developed and applied a charge regulation model to bacterial adhesion and demonstrated that the charge nature of the adhering surface can have a significant effect on the cell surface pH and ultimately the affect the ATP levels of adhered bacteria. The results indicated that the negatively charged glass surface can result in a two-unit drop in cell surface pH, whereas adhesion to a positively charged amine surface can result in a two-unit rise in pH. The working hypothesis indicates that the negatively charged surface should enhance Delta p and increase cellular ATP, while the positively charged surface should decrease Delta p and decrease ATP, and these results of the hypothesis are directly supported by prior experimental results with both negatively and positively charged surfaces. Overall, these results suggest that the nature of charge on the solid surface can have an impact on the proton motive force and cellular ATP levels.

Variation in bacterial ATP concentration during rapid changes in extracellular pH and implications for the activity of attached bacteria

“…E. coli, B. subtilis and P. putida responded similarly to changes in pH and this is seen by the grouping of their confidence intervals, whereas S. epidermis shows distinct deviation from this grouping. When considered in context with our prior work on the variation in bacterial ATP upon adhesion [1][2][3][4][5], these results suggest that S. epidermis adhesion to acidic surfaces would have no effect on cellular bioenergetics, while its adhesion to basic surfaces will have an enhanced effect compared to other neutrophilic bacteria. This information may be useful in identifying and developing antibacterial materials, coatings and solutions to discourage S. epidermidis colonization of surfaces.…”

“…In recent work, we demonstrated that bacterial attachment to a surface can impact cellular bioenergetics, with the effect related to the types and surface densities of acid/base functional groups on the bacterial and solid surfaces [1][2][3][4][5]. Specifically, we have demonstrated that surfaces with acidic functional groups can enhance bacterial activity, measured as an increase in cellular adenosine triphosphate (ATP), whereas surfaces with basic functional groups can decrease cellular ATP.…”

“…We have experimentally demonstrated that adhesion of bacteria under non-growth conditions results in significant shifts in cellular ATP, and numerical modeling of the charge-regulation effect indicates that these shifts were due to local pH variations up to two units away from the pH of the bulk solution [1][2][3]. Full development of this hypothesis, however, requires development of the relationship describing how cellular ATP concentration responds to external pH shifts under non-growth conditions (process C in Fig.…”

“…Through charge-regulation modeling, we have shown that the local pH at the adhesion interface can drop below pH 5 or rise above pH 9, depending on the acid/base characteristics of the bacterial and solid surfaces [1,2,4]. This is illustrated in Fig.…”

“…The current theory describing this effect is based on the chargeregulated nature of the two surfaces, which results in both charge and electrostatic potential variation as a function of separation distance [1][2][3][4][5][6][7][8][9][10]. When a surface with ionizable groups approaches another surface, electroneutrality requires the counterion concentration to increase in the solution between the surfaces to offset the decrease in inter-spatial volume.…”