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Glycosylation of Staphylococcus aureus cell wall teichoic acid is influenced by environmental conditions.

ABSTRACT: Wall teichoic acid (WTA) are major constituents of Staphylococcus aureus (S. aureus) cell envelopes with important roles in the bacteria's physiology, resistance to antimicrobial molecules, host interaction, virulence and biofilm formation. They consist of ribitol phosphate repeat units in which the ribitol residue is substituted with D-alanine (D-Ala) and N-acetyl-D-glucosamine (GlcNAc). The complete S. aureus WTA biosynthesis pathways was recently revealed with the identification of the two glycosyltransferases, TarM and TarS, respectively responsible for the ?- and ?-GlcNAc anomeric substitutions. We performed structural analyses to characterize WTAs from a panel of 24?S. aureus strains responsible for invasive infections. A majority of the S. aureus strains produced the ?-GlcNAc WTA form in accordance with the presence of the tarS gene in all strains assessed. The ?-GlcNAc anomer was preferentially expressed at the expense of the ?-GlcNAc anomer when grown on stress-inducing culture medium containing high NaCl concentration. Furthermore, WTA glycosylation of the prototype S. aureus Newman strain was characterized in vivo in two different animal models, namely peritonitis and deep wound infection. While the inoculum used to infect animals produced almost exclusively ?-GlcNAc WTA, a complete switch to ?-glycosylation was observed in infected kidneys, livers and muscles. Overall, our data demonstrate that S. aureus WTA glycosylation is strongly influenced by environmental conditions and suggest that ?-GlcNAc WTA may bring competitive advantage in vivo.

SUBMITTER: Mistretta N

PROVIDER: S-EPMC6397182 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Glycosylation of Staphylococcus aureus cell wall teichoic acid is influenced by environmental conditions.

Mistretta Noëlle N Brossaud Marina M Telles Fabienne F Sanchez Violette V Talaga Philippe P Rokbi Bachra B

Scientific reports 20190301 1

Wall teichoic acid (WTA) are major constituents of Staphylococcus aureus (S. aureus) cell envelopes with important roles in the bacteria's physiology, resistance to antimicrobial molecules, host interaction, virulence and biofilm formation. They consist of ribitol phosphate repeat units in which the ribitol residue is substituted with D-alanine (D-Ala) and N-acetyl-D-glucosamine (GlcNAc). The complete S. aureus WTA biosynthesis pathways was recently revealed with the identification of the two gl ...[more]

PMID: 30824758

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Project description:ABSTRACT The major clonal lineages of the human pathogen Staphylococcus aureus produce cell wall-anchored anionic poly-ribitol-phosphate (RboP) wall teichoic acids (WTA) substituted with d-Alanine and N-acetyl-d-glucosamine. The phylogenetically isolated S. aureus ST395 lineage has recently been found to produce a unique poly-glycerol-phosphate (GroP) WTA glycosylated with N-acetyl-d-galactosamine (GalNAc). ST395 clones bear putative WTA biosynthesis genes on a novel genetic element probably acquired from coagulase-negative staphylococci (CoNS). We elucidated the ST395 WTA biosynthesis pathway and identified three novel WTA biosynthetic genes, including those encoding an ?-O-GalNAc transferase TagN, a nucleotide sugar epimerase TagV probably required for generation of the activated sugar donor substrate for TagN, and an unusually short GroP WTA polymerase TagF. By using a panel of mutants derived from ST395, the GalNAc residues carried by GroP WTA were found to be required for infection by the ST395-specific bacteriophage ?187 and to play a crucial role in horizontal gene transfer of S. aureus pathogenicity islands (SaPIs). Notably, ectopic expression of ST395 WTA biosynthesis genes rendered normal S. aureus susceptible to ?187 and enabled ?187-mediated SaPI transfer from ST395 to regular S. aureus. We provide evidence that exchange of WTA genes and their combination in variable, mosaic-like gene clusters have shaped the evolution of staphylococci and their capacities to undergo horizontal gene transfer events. IMPORTANCE The structural highly diverse wall teichoic acids (WTA) are cell wall-anchored glycopolymers produced by most Gram-positive bacteria. While most of the dominant Staphylococcus aureus lineages produce poly-ribitol-phosphate WTA, the recently described ST395 lineage produces a distinct poly-glycerol-phosphate WTA type resembling the WTA backbone of coagulase-negative staphylococci (CoNS). Here, we analyzed the ST395 WTA biosynthesis pathway and found new types of WTA biosynthesis genes along with an evolutionary link between ST395 and CoNS, from which the ST395 WTA genes probably originate. The elucidation of ST395 WTA biosynthesis will help to understand how Gram-positive bacteria produce highly variable WTA types and elucidate functional consequences of WTA variation.

Dataset Information

Glycosylation of Staphylococcus aureus cell wall teichoic acid is influenced by environmental conditions.

Publications

Glycosylation of Staphylococcus aureus cell wall teichoic acid is influenced by environmental conditions.

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