Cell Walls of Streptococcus pyogenes, Type 14. C Polysaccharide-Peptidoglycan and G Polysaccharide-Peptidoglycan Complexes

Muñoz, Emilio; Ghuysen, Jean‐Marie; Heymann, H

doi:10.1021/bi00864a007

Cited by 56 publications

(36 citation statements)

References 25 publications

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“…Earlier work had identified LCP proteins as catalysts of WTA and capsular polysaccharide attachment to peptidoglycan (29), specifically the formation of HF-sensitive phosphodiester bonds between the C-6 hydroxyl of N-acetylmuramic acid and WTA or capsular polysaccharide (47)(48)(49). Of note, recent work implicated an LCP-like protein from A. orsi in the glycosylation of a sortase-anchored surface protein, although the chemical nature of the glycosyl modification is still unknown (35).…”

Section: Discussionmentioning

confidence: 99%

LytR-CpsA-Psr Enzymes as Determinants of Bacillus anthracis Secondary Cell Wall Polysaccharide Assembly

et al. 2014

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bBacillus anthracis, the causative agent of anthrax, replicates as chains of vegetative cells by regulating the separation of septal peptidoglycan. Surface (S)-layer proteins and associated proteins (BSLs) function as chain length determinants and bind to the secondary cell wall polysaccharide (SCWP). In this study, we identified the B. anthracis lcpD mutant, which displays increased chain length and S-layer assembly defects due to diminished SCWP attachment to peptidoglycan. In contrast, the B. anthracis lcpB3 variant displayed reduced cell size and chain length, which could be attributed to increased deposition of BSLs. In other bacteria, LytR-CpsA-Psr (LCP) proteins attach wall teichoic acid (WTA) and polysaccharide capsule to peptidoglycan. B. anthracis does not synthesize these polymers, yet its genome encodes six LCP homologues, which, when expressed in S. aureus, promote WTA attachment. We propose a model whereby B. anthracis LCPs promote attachment of SCWP precursors to discrete locations in the peptidoglycan, enabling BSL assembly and regulated separation of septal peptidoglycan. Bacillus anthracis, the causative agent of anthrax, is a sporeforming, Gram-positive bacterium that germinates in host infected tissues and replicates as elongated chains of vegetative forms (1, 2). This unique growth pattern appears to be caused by the regulated separation of septal peptidoglycan, which generates bacterial chains whose mere size precludes clearance by host phagocytes (3-5). The genetic determinants for B. anthracis chain formation are conserved among pathogenic species of the Bacillus cereus group and, as demonstrated with B. cereus G9241, likely contribute to disease pathogenesis (6, 7). Hallmarks of pathogenic Bacillus species are virulence plasmids, pXO-1 and pXO-2 in B. anthracis (8, 9), providing for toxin production and capsulation (10, 11) as well as the chromosomally encoded surface (S)-layer locus (12). Two S-layer proteins of B. anthracis, Sap and EA1, are endowed with S-layer homology (SLH) domains, which retain these proteins in the bacterial envelope by binding to the secondary cell wall polysaccharide (SCWP) (13-15). S-layer protein crystallization domains, responsible for the spontaneous assembly of these polypeptides into a paracrystalline array (16), form a twodimensional lattice that can be thought of as bacterial integument (17)(18)(19).The structural genes of S-layer proteins, sap and eag, are flanked by genes encoding determinants for S-layer protein secretion (secA2 and slaP) (12) or pyruvylation (csaB) (14) as well as acetylation of the SCWP (patA1/2 and patB1/2) (20). CsaB-mediated pyruvylation of the terminal N-acetylmannosamine (ManNAc) of the SCWP (21), with the repeat struc- (22), is a prerequisite for the assembly of S-layer proteins and 22 B. anthracis S-layer-associated proteins (BSLs) (14). PatAB1/2-mediated acetylation of SCWP molecules affects the assembly of EA1 and of some but not all BSLs (20). Recent studies have begun to identify genes for SCWP synthesis, which, unlike py...

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Section: Discussionmentioning

confidence: 99%

LytR-CpsA-Psr Enzymes as Determinants of Bacillus anthracis Secondary Cell Wall Polysaccharide Assembly

et al. 2014

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“…Peptidoglycan also functions as a scaffold for the immobilization of capsular polysaccharides (2), wall teichoic acids (WTAs) (3), and proteins (4). Surface proteins are anchored by sortase A, a membrane-embedded transpeptidase that scans secreted polypeptides for the LPXTG motif of sorting signals (5).…”

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confidence: 99%

“…Rbo-P n is tethered to peptidoglycan via the murein linkage unit, GlcNAc-ManNAc-(glycerol phosphate [Gro-P]) [2][3] (17). Synthesis of the murein linkage unit is initiated by TagO (also referred to as TarO), which links UDP-GlcNAc and undecaprenyl phosphate to generate C 55 -PP-GlcNAc (14,18,19).…”

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Staphylococcus aureus Mutants Lacking the LytR-CpsA-Psr Family of Enzymes Release Cell Wall Teichoic Acids into the Extracellular Medium

et al. 2013

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cThe LytR-CpsA-Psr (LCP) proteins are thought to transfer bactoprenol-linked biosynthetic intermediates of wall teichoic acid (WTA) to the peptidoglycan of Gram-positive bacteria. In Bacillus subtilis, mutants lacking all three LCP enzymes do not deposit WTA in the envelope, while Staphylococcus aureus ⌬lcp mutants display impaired growth and reduced levels of envelope phosphate. We show here that the S. aureus ⌬lcp mutant synthesized WTA yet released ribitol phosphate polymers into the extracellular medium. Further, ⌬lcp mutant staphylococci no longer restricted the deposition of LysM-type murein hydrolases to cell division sites, which was associated with defects in cell shape and increased autolysis. Mutations in S. aureus WTA synthesis genes (tagB, tarF, or tarJ2) inhibit growth, which is attributed to the depletion of bactoprenol, an essential component of peptidoglycan synthesis (lipid II). The growth defect of S. aureus tagB and tarFJ mutants was alleviated by inhibition of WTA synthesis with tunicamycin, whereas the growth defect of the ⌬lcp mutant was not relieved by tunicamycin treatment or by mutation of tagO, whose product catalyzes the first committed step of WTA synthesis. Further, sortase A-mediated anchoring of proteins to peptidoglycan, which also involves bactoprenol and lipid II, was not impaired in the ⌬lcp mutant. We propose a model whereby the S. aureus ⌬lcp mutant, defective in tethering WTA to the cell wall, cleaves WTA synthesis intermediates, releasing ribitol phosphate into the medium and recycling bactoprenol for peptidoglycan synthesis.

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“…S. aureus peptidoglycan (murein) comprises glycan strands with the repeating disaccharide N-acetylmuramic acid (␤1-4)-N-acetylglucosamine (MurNac-GlcNac) units of various lengths (18,19). Short wall peptides, composed of L-Ala-D-iGln-L-Lys-D-Ala, are linked via an amide bond to the D-lactyl moiety of MurNac (20,44,70). Neighboring wall peptides are cross-linked between the ε-amino group of L-Lys in one peptide and the carboxyl group of D-Ala in another via pentaglycine cross bridges.…”

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Cross-Linked Peptidoglycan Mediates Lysostaphin Binding to the Cell Wall Envelope ofStaphylococcus aureus

2006

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Staphylococcus simulans bv. staphylolyticus secretes lysostaphin, a bacteriocin that cleaves pentaglycine cross bridges in the cell wall of Staphylococcus aureus. The C-terminal cell wall-targeting domain (CWT) of lysostaphin is required for selective binding of this bacteriocin to S. aureus cells; however, the molecular target for this was unknown. We used purified green fluorescent protein fused to CWT (GFP-CWT) to reveal speciesspecific association of the reporter with staphylococci. GFP-CWT bound S. aureus cells as well as purified peptidoglycan sacculi. The addition of cross-linked murein, disaccharides linked to interconnected wall peptides, blocked GFP-CWT binding to staphylococci, whereas murein monomers or lysostaphin-solubilized cell wall fragments did not. S. aureus strain Newman variants lacking the capacity for synthesizing polysaccharide capsule (capFO), poly-N-acetylglucosamine (icaAC), lipoprotein (lgt), cell wall-anchored proteins (srtA), or the glycolipid anchor of lipoteichoic acid (ypfP) bound GFP-CWT similar to wild-type staphylococci. A tagO mutant strain, defective in the synthesis of polyribitol wall teichoic acid attached to the cell wall envelope, displayed increased GFP-CWT binding. In contrast, a femAB mutation, reducing both the amount and the length of peptidoglycan cross-linking (monoglycine cross bridges), showed a dramatic reduction in GFP-CWT binding. Thus, the CWT domain of lysostaphin directs the bacteriocin to cross-linked peptidoglycan, which also serves as the substrate for its glycyl-glycine endopeptidase domain.

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Cell Walls of Streptococcus pyogenes, Type 14. C Polysaccharide-Peptidoglycan and G Polysaccharide-Peptidoglycan Complexes

Cited by 56 publications

References 25 publications

LytR-CpsA-Psr Enzymes as Determinants of Bacillus anthracis Secondary Cell Wall Polysaccharide Assembly

LytR-CpsA-Psr Enzymes as Determinants of Bacillus anthracis Secondary Cell Wall Polysaccharide Assembly

Staphylococcus aureus Mutants Lacking the LytR-CpsA-Psr Family of Enzymes Release Cell Wall Teichoic Acids into the Extracellular Medium

Cross-Linked Peptidoglycan Mediates Lysostaphin Binding to the Cell Wall Envelope ofStaphylococcus aureus

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