Teichoic Acid Polymers Affect Expression and Localization of dl -Endopeptidase LytE Required for Lateral Cell Wall Hydrolysis in Bacillus subtilis

Abstract

In Bacillus subtilis, the DL-endopeptidase LytE is responsible for lateral peptidoglycan hydrolysis during cell elongation. We found that I -dependent transcription of lytE is considerably enhanced in a strain with a mutation in ltaS, which encodes a major lipoteichoic acid (LTA) synthase. Similar enhancements were observed in mutants that affect the glycolipid anchor and wall teichoic acid (WTA) synthetic pathways. Immunofluorescence microscopy revealed that the LytE foci were considerably increased in these mutants. The localization patterns of LytE on the sidewalls appeared to be helix-like in LTA-defective or WTAreduced cells and evenly distributed on WTA-depleted or -defective cell surfaces. These results strongly suggested that LTA and WTA affect both I -dependent expression and localization of LytE. Interestingly, increased LytE localization along the sidewall in the ltaS mutant largely occurred in an MreBH-independent manner. Moreover, we found that cell surface decorations with LTA and WTA are gradually reduced at increased culture temperatures and that LTA rather than WTA on the cell surface is reduced at high temperatures. In contrast, the amount of LytE on the cell surface gradually increased under heat stress conditions. Taken together, these results indicated that reductions in these anionic polymers at high temperatures might give rise to increases in SigI-dependent expression and cell surface localization of LytE at high temperatures. IMPORTANCEThe bacterial cell wall is required for maintaining cell shape and bearing environmental stresses. The Gram-positive cell wall consists of mesh-like peptidoglycan and covalently linked wall teichoic acid and lipoteichoic acid polymers. It is important to determine if these anionic polymers are required for proliferation and environmental adaptation. Here, we demonstrated that these polymers affect the expression and localization of a peptidoglycan hydrolase LytE required for lateral cell wall elongation. Moreover, we found that cell surface decorations with teichoic acid polymers are substantially decreased at high temperatures and that the peptidoglycan hydrolase is consequently increased. These findings suggest that teichoic acid polymers control lateral peptidoglycan hydrolysis by LytE, and bacteria drastically change their cell wall content to adapt to their environment.

Streptococcus mutans requires mature rhamnose‐glucose polysaccharides for proper pathophysiology, morphogenesis and cellular division

“…Upon more substantial ablation of RGP formation in the ∆ rgpF and ∆ rgpG mutant strains, GbpB was not only mislocalized, but septation was no longer distinct, and instead appeared to form randomly, further evidenced by diffuse Van‐FL staining. Again, these findings are reminiscent of the consequences of the loss of WTA formation, which results in increased binding of cell wall lytic enzymes across the cell, promoting autolysis in both S. aureus and B. subtilis (Schlag et al , ; Biswas et al , ; Kasahara et al , ). Mature WTA densely populates the cell wall in regions apart from the septum, while within the crosswall, these structures are yet immature and less populous.…”

Identification of Two Phosphate Starvation-induced Wall Teichoic Acid Hydrolases Provides First Insights into the Degradative Pathway of a Key Bacterial Cell Wall Component

“…Moreover, we found an impact of WTA turnover on autolytic activity. WTAs regulate such activity by directing the localization of autolysins (48,49) and by promoting a low cell wall pH that is often inhibitory to their action (50). In B. subtilis, however, cell wall binding of the major secreted autolysin, N-acetylmuramoyl-L-alanine amidase is highly dependent on interactions with WTA (45,51,52).…”

Deficiency in Lipoteichoic Acid Synthesis Causes a Failure in Executing the Colony Developmental Program in Bacillus subtilis

“…LtaS activity was previously shown to be required for proper expression and localization of the LytE and LytF cell wall remodeling enzymes in liquid medium (Kiriyama et al, 2014 ; Kasahara et al, 2016 ). lytF , was found to be underexpressed in Δ ltaS cells (Kiriyama et al, 2014 ), yet deleting the gene had no significant effect on colony size or Y shape formation (Figures 6A,B ; Figure S5A ).…”

“…lytF , was found to be underexpressed in Δ ltaS cells (Kiriyama et al, 2014 ), yet deleting the gene had no significant effect on colony size or Y shape formation (Figures 6A,B ; Figure S5A ). On the other hand, lytE was shown to be overexpressed in the absence of ltaS (Kasahara et al, 2016 ). We therefore examined whether deletion of lytE can suppress the Δ ltaS phenotype.…”