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 α- and β-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 β-GlcNAc WTA form in accordance with the presence of the tarS gene in all strains assessed. The β-GlcNAc anomer was preferentially expressed at the expense of the α-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 α-GlcNAc WTA, a complete switch to β-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 β-GlcNAc WTA may bring competitive advantage in vivo .

Mammalian lectin arrays for screening host–microbe interactions

“…8A). The Wood 46 strain of S. aureus lacks protein A and is tarS ϩ /tarM Ϫ , leading to expression of ␤but not ␣-linked surface GlcNAc (37). Similar results were obtained with independent preparations of labeled bacteria.…”

Molecular Characteristics, Virulence Gene and Wall Teichoic Acid Glycosyltransferase Profiles of Staphylococcus aureus: A Multicenter Study in China

“…Of note, glycosylated WTA acts as bacteriophage receptors to mediate interspecies and intergeneric HGT and takes a great part in the pathogen-host immune response. Therefore, WTA has become an attractive drug target to the infection control of S. aureus and other Gram-positive pathogens in recent decades (Winstel et al, 2015;Mistretta et al, 2019;van Dalen et al, 2019). Gerlach et al demonstrated that tarP played a crucial role in the fitness of these lineages and raised concerns of further dissemination by horizontal gene transfer, but the role of this novel RboP-β-1,3-GlcNAc WTA epitope in immune response remained controversial.…”

“…High-throughput WTA structure analysis requires purified WTA specimens and nuclear magnetic resonance (NMR) spectroscopy, making the identification of WTA glycosylation patterns both time-consuming and laborious. The presence of the glycosyltransferase genes in S. aureus isolates which can be easily detected by PCR has been generally used to infer their WTA glycosylation patterns (Mistretta et al, 2019). Therefore, the investigation of WTA glycosyltransferase gene profiles may contribute to understanding the genetic diversification and the emergence of new pathogenic strains in S. aureus.…”

High‐throughput transposon sequencing highlights the cell wall as an important barrier for osmotic stress in methicillin resistant Staphylococcus aureus and underlines a tailored response to different osmotic stressors

“…Nevertheless, several possible changes to the cell wall have been observed in S. aureus during NaCl stress, such as shortened interpeptide bridges in the peptidoglycan (Vijaranakul et al, ), an increase in resistance to methicillin (Madiraju, Brunner, & Wilkinson, ) and increased autolysis activity (Ochiai, ; Stapleton et al, ). In addition to peptidoglycan, other components within the cell envelope, such as teichoic acids and more specifically their modifications with D‐alanine (Koprivnjak et al, ) and sugar residues (Kho & Meredith, ; Mistretta et al, ) are affected by osmotic stress. Combined, these findings indicate that the integrity of the cell wall is an important requirement for osmotic resistance.…”