The heat-inducible essential response regulator WalR positively regulates transcription of sigI, mreBH and lytE in Bacillus subtilis under heat stress

Huang, Wan-Zhen; Wang, Jyun-Jhih; Chen, Hui-Ju; Chen, Jung-Tze; Shaw, Gordon L.

doi:10.1016/j.resmic.2013.10.003

Cited by 18 publications

(19 citation statements)

References 32 publications

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“…S1B in the supplemental material). A similar enhancement of lytE transcription has been reported under heat stress (17,41). Therefore, we assessed LytE localization at high temperatures and found that the amount of LytE in the cell surface fractions gradually increased under heat stress (Fig.…”

Section: Resultssupporting

confidence: 81%

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

et al. 2016

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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.

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Section: Resultssupporting

confidence: 81%

“…Notably, SigI is required for most lytE transcription, and the DL-endopeptidase activity of LytE is essential for survival under heat stress (17,41). In this report, we found that loss of the poly(GroP) main chains of LTA or WTA at 37°C affects the expression of lytE and mreBH, which are part of the SigI regulon ( Fig.…”

Section: Discussionmentioning

confidence: 58%

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

et al. 2016

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“…In S. aureus and S. pneumoniae YycFG also regulates genes involved in metabolism, stress response, virulence, multidrug resistance, host–microbe interactions and other regulatory pathways (Dubrac and Msadek, 2004; Mohedano et al, 2005; Howden et al, 2011; Delaune et al, 2012; Huang et al, 2013). There is also evidence that YycFG plays a role in membrane synthesis in several bacteria, thereby regulating membrane fluidity and permeability.…”

Section: Introductionmentioning

confidence: 99%

The Response Regulator YycF Inhibits Expression of the Fatty Acid Biosynthesis Repressor FabT in Streptococcus pneumoniae

et al. 2016

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The YycFG (also known as WalRK, VicRK, MicAB, or TCS02) two-component system (TCS) is highly conserved among Gram-positive bacteria with a low G+C content. In Streptococcus pneumoniae the YycF response regulator has been reported to be essential due to its control of pcsB gene expression. Previously we showed that overexpression of yycF in S. pneumoniae TIGR4 altered the transcription of genes involved in cell wall metabolism and fatty acid biosynthesis, giving rise to anomalous cell division and increased chain length of membrane fatty acids. Here, we have overexpressed the yycFG system in TIGR4 wild-type strain and yycF in a TIGR4 mutant depleted of YycG, and analyzed their effects on expression of proteins involved in fatty acid biosynthesis during activation of the TCS. We demonstrate that transcription of the fab genes and levels of their products were only altered in the YycF overexpressing strain, indicating that the unphosphorylated form of YycF is involved in the regulation of fatty acid biosynthesis. In addition, DNA-binding assays and in vitro transcription experiments with purified YycF and the promoter region of the FabTH-acp operon support a direct inhibition of transcription of the FabT repressor by YycF, thus confirming the role of the unphosphorylated form in transcriptional regulation.

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“…During phosphate starvation, the two-component system PhoPR of Bacillus subtilis activates transcription of APase genes (phoA, phoB, and phoD) to generate free phosphate groups for uptake and utilization (Allenby et al, 2005;Antelmann et al, 2000). Among the vegetatively expressed cell wall hydrolase genes lytC, lytD, lytE, lytF, cwlO, and cwlS of B. subtilis, only lytE and cwlO are not regulated by SigD (Chen et al, 2009;Huang et al, 2013;Noone et al, 2014;Tseng et al, 2011). It has been reported that LytE and CwlO are required for cell elongation and that cells lacking both enzymes exhibit a synthetic lethal phenotype (Bisicchia et al, 2007;Hashimoto et al, 2012).…”

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confidence: 99%

“…Given the co-induction of lytE and phoA by heat stress (Helmann et al, 2001;Huang et al, 2013;Tseng et al, 2011) and the co-inhibition of the levels of LytE and PhoA by Spo0A in B. subtilis (Hulett et al, 1994;Jensen et al, 1993;Kodama et al, 2007), we wondered whether there would be other correlation(s) between expression of lytE and phoA. Firstly, effect of mutation of lytE on transcription of phoA was investigated by using PCR and the primer pair A64 plus A65 (Table S1) to construct the pDLbased integrative plasmid pGS2095 (Table 1), which carries a transcriptional fusion of the regulatory region of phoA with bgaB.…”

mentioning

confidence: 99%

Expressions of alkaline phosphatase genes during phosphate starvation are under positive influences of multiple cell wall hydrolase genes in <i>Bacillus subtilis</i>

Shen¹,

Hu²,

Shaw³

2016

J. Gen. Appl. Microbiol.

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The heat-inducible essential response regulator WalR positively regulates transcription of sigI, mreBH and lytE in Bacillus subtilis under heat stress

Cited by 18 publications

References 32 publications

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

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

The Response Regulator YycF Inhibits Expression of the Fatty Acid Biosynthesis Repressor FabT in Streptococcus pneumoniae

Expressions of alkaline phosphatase genes during phosphate starvation are under positive influences of multiple cell wall hydrolase genes in <i>Bacillus subtilis</i>

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