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.Bacterial adhesion and biofilm formation are important to a wide array of fields, such as environmental, chemical, and biomedical engineering; food processing; materials science; marine science; and ecology and environmental sciences. A key consideration in the development of a biofilm is the initial interaction between the bacterium and the substrata and the way in which these interactions affect the metabolic activity of the cells. If the metabolic activity increases, this would help the cells colonize the surface, whereas if the metabolic activity decreases, then the cells may become inactive or die.There have been a number of studies that have examined the effects of attachment on bacterial metabolic activity. The first reported observation of this effect was made in 1943, where it was found that bacterial activity increased in the presence of glass surfaces, particularly with low nutrient concentrations (54). Since this first study, researchers have examined how various materials, including glass and polymer surfaces (10, 11, 24-26, 40, 44, 47), silicone surfaces (52), ceramic surfaces (32), dialysis membranes (18), activated carbon (7), clays (43), sands (31, 48), estuary particles (19), and ion exchange resins (46), affect the metabolic activity of attached bacteria.Different mechanisms have been examined in an attempt to explain how surfaces affect bacterial metabo...

Actin-like cytoskeleton filaments contribute to cell mechanics in bacteria

“…S8). This result is consistent with previous studies that show that starved E. coli cells maintain a significant pool of ATP, about 20%-60% of the total adenylate pool in adhered cells (22). Because murein remodeling is thought to be inhibited in nongrowing cells, these experiments indicate that cell-wall remodeling is not required for the decrease in stiffness upon the addition of A22.…”

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

“…It was previously shown that the ATP levels of both E. coli and B. brevis adhered onto the glass surface were 2-5 times higher than that of corresponding planktonic bacteria (Hong and Brown, 2009). Then, using a bioenergetic model, it was shown that a change in pH in the periplasmic space of only 0.2-0.5 units was required to achieve these changes in ATP levels (Hong and Brown, 2009).…”

“…It was previously shown that the ATP levels of both E. coli and B. brevis adhered onto the glass surface were 2-5 times higher than that of corresponding planktonic bacteria (Hong and Brown, 2009). Then, using a bioenergetic model, it was shown that a change in pH in the periplasmic space of only 0.2-0.5 units was required to achieve these changes in ATP levels (Hong and Brown, 2009). A key question remaining from the earlier study was whether a change in cell surface pH occurs upon adhesion that can result in this required pH change in the periplasmic space (i.e., the pH change at the cell surface is greater than or equal to the change required at the cytoplasmic membrane).…”

“…In a previous study (Hong and Brown, 2009), we demonstrated for two well-characterized bacteria-the Gram-negative Escherichia coli and the Gram-positive Bacillus brevis-that in the absence of any growth substrates, bacteria adhered onto negatively charged glass beads had higher ATP levels per cell than planktonic bacteria. The calculated proton motive force (Dp) of the adhered bacteria was approximately 10-15% greater than the planktonic bacteria, which resulted in the adhered cells having approximately 0.2-0.5 units greater DpH component of Dp than planktonic bacteria.…”

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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 (Dp) of adhered bacteria was approximately 15% greater than that of planktonic bacteria.

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