scholarly journals GpsB coordinates cell division and cell surface decoration by wall teichoic acids in Staphylococcus aureus

2021 ◽  
Author(s):  
Lauren R. Hammond ◽  
Sebastian J. Khan ◽  
Michael D. Sacco ◽  
Catherine Spanoudis ◽  
Abigail Hough ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Cell Division ◽  
Cell Surface ◽  
Teichoic Acid ◽  
Model Organisms ◽  
Bacterial Cell Division ◽  
Human Pathogens ◽  
Wall Teichoic Acid ◽  
Surface Decoration ◽  
Multiple Species

Bacterial cell division is a complex and highly regulated process requiring the coordination of many different proteins. Despite substantial work in model organisms, our understanding of the systems regulating cell division in non-canonical organisms, including critical human pathogens, is far from complete. One such organism is Staphylococcus aureus, a spherical bacterium that lacks known cell division regulatory proteins. Recent studies on GpsB, a protein conserved within the Firmicutes phylum, have provided insight into cell division regulation in S. aureus and other related organisms. It has been revealed that GpsB coordinates cell division and cell wall synthesis in multiple species by interacting with Penicillin Binding Proteins (PBPs) and other partners. In S. aureus, we have previously shown that GpsB directly regulates FtsZ polymerization. In this study, using Bacillus subtilis as a tool, we isolated intragenic and extragenic spontaneous suppressor mutants that abrogate the lethality of S. aureus GpsB overproduction in B. subtilis. Through characterization of these mutants, we identified several key residues important for the function of GpsB. Furthermore, we discovered an additional role for GpsB in wall teichoic acid (WTA) biosynthesis in S. aureus. Specifically, we show that GpsB directly interacts with the wall teichoic acid export protein TarG using a bacterial two-hybrid analysis. We also identified a three-residue motif in GpsB that is crucial for this interaction. Based on the analysis of the localization of TagG in B. subtilis and its homolog TarG in S. aureus, it appears that WTA machinery is a part of the divisome complex. As such, we show additional evidence to the growing body of work that suggests that along with peptidoglycan synthesis, WTA biosynthesis and export may take place at the site of cell division. Taken together, this research illustrates how GpsB performs an essential function in S. aureus by directly linking the tightly regulated cell cycle processes of cell division and WTA-mediated cell surface decoration.

scholarly journals The Staphylococcus aureus Methicillin Resistance Factor FmtA Is a d-Amino Esterase That Acts on Teichoic Acids

mBio ◽  
2016 ◽  
Vol 7 (1) ◽  
Author(s):  
Muhammad M. Rahman ◽  
Howard N. Hunter ◽  
Shamina Prova ◽  
Vidhu Verma ◽  
Aneela Qamar ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Cell Wall ◽  
Cell Division ◽  
Cell Surface ◽  
Biofilm Formation ◽  
Negative Charge ◽  
Methicillin Resistance ◽  
Teichoic Acid ◽  
Teichoic Acids ◽  
Phosphate Backbone

ABSTRACT The methicillin resistance factor encoded by fmtA is a core member of the Staphylococcus aureus cell wall stimulon, but its function has remained elusive for the past two decades. First identified as a factor that affects methicillin resistance in S. aureus strains, FmtA was later shown to interact with teichoic acids and to localize to the cell division septum. We have made a breakthrough in understanding FmtA function. We show that FmtA hydrolyzes the ester bond between d -Ala and the backbone of teichoic acids, which are polyglycerol-phosphate or polyribitol-phosphate polymers found in the S. aureus cell envelope. FmtA contains two conserved motifs found in serine active-site penicillin-binding proteins (PBPs) and β-lactamases. The conserved SXXK motif was found to be important for the d -amino esterase activity of FmtA. Moreover, we show that deletion of fmtA (Δ fmtA ) led to higher levels of d -Ala in teichoic acids, and this effect was reversed by complementation of Δ fmtA with fmtA . The positive charge on d -Ala partially masks the negative charge of the polyol-phosphate backbone of teichoic acids; hence, a change in the d -Ala content will result in modulation of their charge. Cell division, biofilm formation, autolysis, and colonization are among the many processes in S. aureus affected by the d -Ala content and overall charge of the cell surface teichoic acids. The esterase activity of FmtA and the regulation of fmtA suggest that FmtA functions as a modulator of teichoic acid charge, thus FmtA may be involved in S. aureus cell division, biofilm formation, autolysis, and colonization. IMPORTANCE Teichoic acids are involved in cell division, cell wall synthesis, biofilm formation, attachment of bacteria to artificial surfaces, and colonization. However, the function of teichoic acids is not fully understood. Modification by glycosylation and/or d -alanylation of the polyol-phosphate backbone of teichoic acids is important in the above cell processes. The intrinsic negative charge of teichoic acid backbone plays a role in the charge and/or pH of the bacterial surface, and d -alanylation represents a means through which bacteria modulate the charge or the pH of their surfaces. We discovered that FmtA removes d -Ala from teichoic acids. We propose FmtA may provide a temporal and spatial regulation of the bacterial cell surface charge in two ways, by removing the d -Ala from LTA to make it available to wall teichoic acid (WTA) in response to certain conditions and by removing it from WTA to allow the cell to reset its surface charge to a previous condition.

scholarly journals Non-protein components of the cell surface of Staphylococcus aureus

1968 ◽  
Vol 107 (6) ◽  
pp. 817-821 ◽  
Author(s):  
A. M. James ◽  
J. E. Brewer
Keyword(s):  
Staphylococcus Aureus ◽  
Cell Surface ◽  
Teichoic Acid ◽  
Surface Damage ◽  
Sodium Metaperiodate ◽  
Maximum Value ◽  
Dependent Change ◽  
Ph Dependent ◽  
Pass Through ◽  
Protein Components

1. pH–mobility curves of various laboratory strains of Staphylococcus aureus are non-sigmoid in shape, and all pass through a maximum value in the range pH4–5. 2. The maxima in the curves are not due to incomplete washing of the cells, adsorption of buffer components or irreversible surface damage. 3. Mild oxidation of the cell-surface teichoic acid with sodium metaperiodate gives cells that have typical sigmoid pH–mobility curves, characteristic of either a simple carboxyl surface or a mixed carboxyl–amino surface. 4. The results are discussed in terms of a pH-dependent change in the configuration of the teichoic acid molecules at the surface.

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

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Noëlle Mistretta ◽  
Marina Brossaud ◽  
Fabienne Telles ◽  
Violette Sanchez ◽  
Philippe Talaga ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Cell Wall ◽  
Environmental Conditions ◽  
Teichoic Acid ◽  
Wall Teichoic Acid

scholarly journals Surface Glycopolymers Are Crucial forIn VitroAnti-Wall Teichoic Acid IgG-Mediated Complement Activation and Opsonophagocytosis of Staphylococcus aureus

2015 ◽  
Vol 83 (11) ◽  
pp. 4247-4255 ◽  
Author(s):  
Jong-Ho Lee ◽  
Na-Hyang Kim ◽  
Volker Winstel ◽  
Kenji Kurokawa ◽  
Jesper Larsen ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Teichoic Acid ◽  
Complement C3 ◽  
Glycerol Phosphate ◽  
Glycosylation Pattern ◽  
Wall Teichoic Acid ◽  
Content Type ◽  
Gram Positive Bacteria ◽  
Capsule Production ◽  
Cell Envelopes

ABSTRACTThe cell envelopes of many Gram-positive bacteria contain wall teichoic acids (WTAs).Staphylococcus aureusWTAs are composed of ribitol phosphate (RboP) or glycerol phosphate (GroP) backbones substituted withd-alanine andN-acetyl-d-glucosamine (GlcNAc) orN-acetyl-d-galactosamine (GalNAc). Two WTA glycosyltransferases, TarM and TarS, are responsible for modifying the RboP WTA with α-GlcNAc and β-GlcNAc, respectively. We recently reported that purified human serum anti-WTA IgG specifically recognizes β-GlcNAc of the staphylococcal RboP WTA and then facilitates complement C3 deposition and opsonophagocytosis ofS. aureuslaboratory strains. This prompted us to examine whether anti-WTA IgG can induce C3 deposition on a diverse set of clinicalS. aureusisolates. To this end, we compared anti-WTA IgG-mediated C3 deposition and opsonophagocytosis abilities using 13 different staphylococcal strains. Of note, the majority ofS. aureusstrains tested was recognized by anti-WTA IgG, resulting in C3 deposition and opsonophagocytosis. A minority of strains was not recognized by anti-WTA IgG, which correlated with either extensive capsule production or an alteration in the WTA glycosylation pattern. Our results demonstrate that the presence of WTAs with TarS-mediated glycosylation with β-GlcNAc in clinically isolatedS. aureusstrains is an important factor for induction of anti-WTA IgG-mediated C3 deposition and opsonophagocytosis.

scholarly journals Wall teichoic acid protects Staphylococcus aureus from inhibition by Congo red and other dyes

2012 ◽  
Vol 67 (9) ◽  
pp. 2143-2151 ◽  
Author(s):  
T. Suzuki ◽  
J. Campbell ◽  
Y. Kim ◽  
J. G. Swoboda ◽  
E. Mylonakis ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Congo Red ◽  
Teichoic Acid ◽  
Wall Teichoic Acid

scholarly journals Isolation and Characterization of Biofilm Formation-Defective Mutants of Staphylococcus aureus

2006 ◽  
Vol 75 (3) ◽  
pp. 1079-1088 ◽  
Author(s):  
Patrick H. Tu Quoc ◽  
Pierre Genevaux ◽  
Maria Pajunen ◽  
Harri Savilahti ◽  
Costa Georgopoulos ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Biofilm Formation ◽  
Teichoic Acid ◽  
Hypothetical Protein ◽  
Inducible Promoter ◽  
Clinical Strain ◽  
High Morbidity ◽  
Wall Teichoic Acid ◽  
Comprehensive Collection ◽  
Isolation And Characterization

ABSTRACT Staphylococcus aureus produces biofilm and this mode of colonization facilitates infections that are often difficult to treat and engender high morbidity and mortality. We have exploited bacteriophage Mu transposition methods to create an insertional mutant library in a highly biofilm-forming S. aureus clinical isolate. Our screen identified 38 insertions in 23 distinct genes together with one intergenic region that significantly reduced biofilm formation. Nineteen insertions were mapped in loci not previously known to affect biofilm in this organism. These include insertions in codY, srrA, mgrA, and fmtA, a putative DEAD-box helicase, two members of the zinc-metallo-β lactamase/β-CASP family, and a hypothetical protein with a GGDEF motif. Fifteen insertions occurred in the icaADBC operon, which produces intercellular adhesion antigen (PIA) and is important for biofilm formation in many strains of S. aureus and Staphylococcus epidermidis. Obtaining a high proportion of independent Em-Mu disruptions in icaADBC demonstrated both the importance of PIA for biofilm formation in this clinical strain and the strong validation of the screening procedure that concomitantly uncovered additional mutants. All non-ica mutants were further analyzed by immunoblotting and biochemical fractionation for perturbation of PIA and wall teichoic acid. PIA levels were diminished in the majority of non-ica insertional mutants. Three mutant strains were chosen and were functionally complemented for restored biofilm formation by transformation with plasmids carrying the cloned wild-type gene under the control of a xylose-inducible promoter. This is a comprehensive collection of biofilm-defective mutants that underscores the multifactorial genetic program underlying the establishment of biofilm in this insidious pathogen.

scholarly journals Wall Teichoic Acid Glycosylation Governs Staphylococcus aureus Nasal Colonization

mBio ◽  
2015 ◽  
Vol 6 (4) ◽  
Author(s):  
Volker Winstel ◽  
Petra Kühner ◽  
Ferdinand Salomon ◽  
Jesper Larsen ◽  
Robert Skov ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Risk Factor ◽  
Epithelial Cells ◽  
Teichoic Acid ◽  
Nasal Colonization ◽  
Human Pathogen ◽  
Wall Teichoic Acid ◽  
Content Type ◽  
Human Nasal Epithelial Cells ◽  
Key Factor

ABSTRACT Nasal colonization by the human pathogen Staphylococcus aureus is a major risk factor for hospital- and community-acquired infections. A key factor required for nasal colonization is a cell surface-exposed zwitterionic glycopolymer, termed wall teichoic acid (WTA). However, the precise mechanisms that govern WTA-mediated nasal colonization have remained elusive. Here, we report that WTA GlcNAcylation is a pivotal requirement for WTA-dependent attachment of community-acquired methicillin-resistant S. aureus (MRSA) and emerging livestock-associated MRSA to human nasal epithelial cells, even under conditions simulating the nutrient composition and dynamic flow of nasal secretions. Depending on the S. aureus strain, WTA O-GlcNAcylation occurs in either α or β configuration, which have similar capacities to mediate attachment to human nasal epithelial cells, suggesting that many S. aureus strains maintain redundant pathways to ensure appropriate WTA glycosylation. Strikingly, a lack of WTA glycosylation significantly abrogated the ability of MRSA to colonize cotton rat nares in vivo. These results indicate that WTA glycosylation modulates S. aureus nasal colonization and may help to develop new strategies for eradicating S. aureus nasal colonization in the future. IMPORTANCE Nasal colonization by the major human pathogen Staphylococcus aureus is a risk factor for severe endogenous infections and contributes to the spread of this microbe in hospitals and the community. Here, we show that wall teichoic acid (WTA) O-GlcNAcylation is a key factor required for S. aureus nasal colonization. These data provide a mechanistic explanation for the capacity of WTA to modulate S. aureus nasal colonization and may stimulate research activities to establish valuable strategies to eradicate S. aureus nasal colonization in high-risk hospitalized patients and in the general community.

scholarly journals Wall Teichoic Acid Protects Staphylococcus aureus against Antimicrobial Fatty Acids from Human Skin

2009 ◽  
Vol 191 (13) ◽  
pp. 4482-4484 ◽  
Author(s):  
Thomas Kohler ◽  
Christopher Weidenmaier ◽  
Andreas Peschel
Keyword(s):  
Fatty Acids ◽  
Staphylococcus Aureus ◽  
Fatty Acid ◽  
Teichoic Acid ◽  
Sebaceous Glands ◽  
Wall Teichoic Acid ◽  
Fatty Acid Binding ◽  
Gram Positive Bacteria ◽  
Skin Colonization ◽  
Wall Teichoic Acids

ABSTRACT Skin-colonizing gram-positive bacteria produce wall teichoic acids (WTAs) or related glycopolymers for unclear reasons. Using a WTA-deficient Staphylococcus aureus mutant, we demonstrated that WTA confers resistance to antimicrobial fatty acids from human sebaceous glands by preventing fatty acid binding. Thus, WTA is probably important for bacterial skin colonization.

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