Proton-binding capacity of Staphylococcus aureus wall teichoic acid and its role in controlling autolysin activity

Abstract

Wall teichoic acid (WTA) or related polyanionic cell wall glycopolymers are produced by most gram-positive bacterial species and have been implicated in various cellular functions. WTA and the proton gradient across bacterial membranes are known to control the activity of autolysins but the molecular details of these interactions are poorly understood. We demonstrate that WTA contributes substantially to the proton-binding capacity of Staphylococcus aureus cell walls and controls autolysis largely via the major autolysin AtlA whose activity is known to decline at acidic pH values. Compounds that increase or decrease the activity of the respiratory chain, a main source of protons in the cell wall, modulated autolysis rates in WTA-producing cells but did not affect the augmented autolytic activity observed in a WTA-deficient mutant. We propose that WTA represents a cation-exchanger like mesh in the gram-positive cell envelopes that is required for creating a locally acidified milieu to govern the pH-dependent activity of autolysins.

Figure 1. Increased autolysis of S. aureus ΔtagO depends on the major autolysin AtlA.

AtlA-expressing or deficient strains are indicated by continuous or dotted lines, respectively. Means and SEM of 3 independent experiments are shown.

Figure 2. Autolysis can be increased by addition of azide or inhibited by addition of glucose in WTA-containing but not in WTA-deficient S. aureus.

Means and SEM of 3 independent experiments are shown. Between-group differences were analyzed for significance by one-way ANOVA analysis. *, p<0.05; ***, p<0.001; ns, not significant.

Figure 3. Model for the role of WTA in proton binding and control of autolysin activity.

(A) The negatively charged WTA phosphate groups retain protons in the cell wall, which creates an acidic environment keeping the activity of the major autolysin AtlA low. (B) In the absence of WTA protons are not retained, which avoids local acidification and leads to higher activity of AtlA.