Regulation of LiaRS-Dependent Gene Expression in<i>Bacillus subtilis</i>: Identification of Inhibitor Proteins, Regulator Binding Sites, and Target Genes of a Conserved Cell Envelope Stress-Sensing Two-Component System

Jordan, Sina; Junker, Albrecht; Helmann, John D.; Mascher, Thorsten

doi:10.1128/jb.00310-06

Cited by 197 publications

(357 citation statements)

References 62 publications

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“…Our results indicate that SpxB is a novel positive regulator of OatA expression. Interestingly, the spxB promoter region contains a sequence similar to that reportedly recognized by the TCS LiaRS in B. subtilis (38) or CesSR in L. lactis. 10 Both TCSs are members of the envelope stress sensor family and mediate the cellular response to cell wall synthesis-directed antimicrobial treatments in low G ϩ C Gram-positive bacteria (37, 46 -48).…”

Section: Discussionmentioning

confidence: 79%

“…The homology of SpxB to both TrmA and B. subtilis Spx further suggested its possible regulatory function. By means of MEME motif software (36), we detected a sequence in the spxB promoter region that is similar to a sequence reportedly regulating the expression of the two-component system (TCS) LiaRS in B. subtilis (37,38) or CesSR in L. lactis, 10 both of which respond to cell envelope stress (Fig. 1).…”

Section: Overexpression Of Pgda and Spxb (Yneh) Confers Lactococcalmentioning

confidence: 92%

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SpxB Regulates O-Acetylation-dependent Resistance of Lactococcus lactis Peptidoglycan to Hydrolysis

Veiga

Bulbarela-Sampieri

Furlan

et al. 2007

Journal of Biological Chemistry

105

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Endogenous peptidoglycan (PG)-hydrolyzing enzymes, the autolysins, are needed to relax the rigid PG sacculus to allow bacterial cell growth and separation. PGs of pathogens and commensal bacteria may also be degraded by hydrolases of animal origin (lysozymes), which act as antimicrobials. The genetic mechanisms regulating PG resistance to hydrolytic degradation were dissected in the Gram-positive bacterium Lactococcus lactis. We found that the ability of L. lactis to counteract PG hydrolysis depends on the degree of acetylation. Overexpression of PG O-acetylase (encoded by oatA) led to bacterial growth arrest, indicating the potential lethality of oatA and a need for its tight regulation. A novel regulatory factor, SpxB (previously denoted as YneH), exerted a positive effect on oatA expression. Our results indicate that SpxB binding to RNA polymerase constitutes a previously missing link in the multistep response to cell envelope stress, provoked by PG hydrolysis with lysozyme. We suggest that the two-component system CesSR responds to this stress by inducing SpxB, thus favoring its interactions with RNA polymerase. Induction of PG O-acetylation by this cascade renders it resistant to hydrolysis. Peptidoglycan (PG)7 is the major and essential component of the bacterial cell envelope, the main function of which is to preserve cell integrity by withstanding internal osmotic pressure (1, 2). It is also responsible for cell shape, participates in cell division, and serves as support for attachment of other cell wall molecules such as teichoic acids, proteins, and exopolysaccharides (3). The bacterial PG is a giant multilayer polymer that envelops the cell as a rigid sacculus. It is composed of N-acetylglucosamine-N-acetylmuramic acid disaccharide pentapeptide blocks that are synthesized intracellularly and transported through the cytoplasmic membrane as lipid-disaccharide pentapeptides. These blocks are covalently linked to the pre-existing PG polymers by high molecular weight penicillin-binding proteins (4).To allow cell division and surface expansion, the rigid PG sacculus has to be relaxed. This is achieved by PG ruptures, which could be introduced in several ways. First, not all possible covalent bonds are formed during PG synthesis; for example, only 36% of possible PG cross-links between stem peptides are formed in Lactococcus lactis (5). Bacteria also possess a number of endogenous bacterial enzymes (collectively called autolysins) that disrupt PG and can result in cell lysis. According to their hydrolytic bond specificity and products, autolysins are classified as muramidases, lytic transglycosylases, glucosaminidases, amidases, and peptidases (6). Bacteria often possess several autolysins, e.g. L. lactis encodes a main autolysin (N-acetylglucosaminidase AcmA) (7, 8) and four minor PG hydrolases (9, 10) as well as prophage-encoded bacteriolytic enzymes (11).In the human or animal host, antimicrobial PG lytic enzymes such as lysozyme constitute a first line of defense against infection. Bactericidal propertie...

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Section: Discussionmentioning

confidence: 79%

Section: Overexpression Of Pgda and Spxb (Yneh) Confers Lactococcalmentioning

confidence: 92%

SpxB Regulates O-Acetylation-dependent Resistance of Lactococcus lactis Peptidoglycan to Hydrolysis

Veiga

Bulbarela-Sampieri

Furlan

et al. 2007

Journal of Biological Chemistry

105

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“…For example, LiaRS-like systems respond to a variety of cell envelope-damaging agents and usually, but not always, confer resistance to them. 133,141 However, the identity and extent of their target genes varies considerably between species. Another example more pertinent for this review is the ApsXRS/GraXRS system, studied most in staphylococci and streptococci, which responds to CAMPs.…”

Section: Introduction To Gram-positive Esrsmentioning

confidence: 99%

Regulation of bacterial virulence gene expression by cell envelope stress responses

Flores-Kim

Darwin

2014

Virulence

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“…The cell envelope stress LiaSR two-component regulatory system is widespread among the Firmicutes (Jordan et al, 2006(Jordan et al, , 2008. LiaS is an intramembrane-sensing histidine kinase and believed to sense signals that perturb membrane damage.…”

Section: Introductionmentioning

confidence: 99%

Regulation of d-alanylation of lipoteichoic acid in Streptococcus gordonii

et al. 2011

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D-Alanyl esters on lipoteichoic acid (LTA) are involved in adhesion, biofilm formation, resistance to cationic antimicrobial peptides, and immune stimulation. There is evidence that bacteria can modulate the level of D-alanyl esters on LTA in response to challenge, but the mechanism of regulation appears to be different among bacteria. In this study, expression of the dlt operon responsible for D-alanylation of LTA was examined in the commensal bacterium Streptococcus gordonii. dlt expression was assessed using the dlt promoter-lacZ reporter gene assay, LTA D-alanine content measurements and dlt mRNA quantification. The results showed that dlt expression was growth phase-dependent, with the greatest expression at the mid-exponential phase of growth. In contrast to Staphylococcus aureus, dlt expression in Strep. gordonii was not affected by the exogenous addition of Mg 2+ or K + . Interestingly, dlt expression was upregulated under acidic conditions or when cells were stressed with polymyxin B, indicating that cell envelope stress may be a signal for dlt expression. In view of these results, mutants defective in the cell envelope stress LiaSR two-component regulatory system were constructed. The liaS and liaR mutants showed an increase in dlt expression over the parent strain at neutral pH. The mutants failed to respond to low pH and polymyxin B stress; dlt expression remained the same in the presence or absence of these stresses. These results suggest that dlt expression in Strep. gordonii is regulated by the LiaSR regulatory system in response to environmental signals such as pH and polymyxin B. The regulation appears to be complex, involving both repression and activation mechanisms. INTRODUCTIONLipoteichoic acid (LTA) is an amphiphilic polymer of polyphosphoglycerol or polyphosphoribitol anchored to the cytoplasmic membrane by a glycolipid. Each phosphoglycerol or phosphoribitol on this molecule may be modified by glycosylation or, more often, substituted with D-alanyl esters (Fischer, 1988;Fischer et al., 1990). The dlt operon is responsible for the D-alanylation of LTA (Neuhaus & Baddiley, 2003). The operon consists of four genes, dltA, dltB, dltC and dltD. The dltA gene encodes the D-alanyl carrier protein ligase (Dcl), which activates the D-alanine and ligates it to the D-alanyl carrier protein (Dcp). The function of the protein encoded by dltB has not been experimentally established, but it is a transport protein that is thought to serve as a channel to secrete the unfolded D-alanyl Dcp. The dltD gene encodes a membraneassociated protein, which facilitates the binding of Dcp and Dcl for ligation of Dcp with D-alanine. Disruption of any one of the dlt genes will eliminate D-alanylation of LTA.D-Alanylation confers a positive charge upon LTA and has been demonstrated to have a role in the regulation of autolytic activity (Fischer et al., 1981), the binding of Mg 2+ (Archibald et al., 1973), intragenic coaggregation (Clemans et al., 1999), biofilm formation (Fabretti et al., 2006;Gross et al., 2001), adhere...

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Regulation of LiaRS-Dependent Gene Expression inBacillus subtilis: Identification of Inhibitor Proteins, Regulator Binding Sites, and Target Genes of a Conserved Cell Envelope Stress-Sensing Two-Component System

Cited by 197 publications

References 62 publications

SpxB Regulates O-Acetylation-dependent Resistance of Lactococcus lactis Peptidoglycan to Hydrolysis

SpxB Regulates O-Acetylation-dependent Resistance of Lactococcus lactis Peptidoglycan to Hydrolysis

Regulation of bacterial virulence gene expression by cell envelope stress responses

Regulation of d-alanylation of lipoteichoic acid in Streptococcus gordonii

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