scholarly journals Teichoic Acid Is an Essential Polymer in Bacillus subtilis That Is Functionally Distinct from Teichuronic Acid

2004 ◽  
Vol 186 (23) ◽  
pp. 7865-7873 ◽  
Author(s):  
Amit P. Bhavsar ◽  
Laura K. Erdman ◽  
Jeffrey W. Schertzer ◽  
Eric D. Brown

ABSTRACT Wall teichoic acids are anionic, phosphate-rich polymers linked to the peptidoglycan of gram-positive bacteria. In Bacillus subtilis, the predominant wall teichoic acid types are poly(glycerol phosphate) in strain 168 and poly(ribitol phosphate) in strain W23, and they are synthesized by the tag and tar gene products, respectively. Growing evidence suggests that wall teichoic acids are essential in B. subtilis; however, it is widely believed that teichoic acids are dispensable under phosphate-limiting conditions. In the work reported here, we carefully studied the dispensability of teichoic acid under phosphate-limiting conditions by constructing three new mutants. These strains, having precise deletions in tagB, tagF, and tarD, were dependent on xylose-inducible complementation from a distal locus (amyE) for growth. The tarD deletion interrupted poly(ribitol phosphate) synthesis in B. subtilis and represents a unique deletion of a tar gene. When teichoic acid biosynthetic proteins were depleted, the mutants showed a coccoid morphology and cell wall thickening. The new wall teichoic acid biogenesis mutants generated in this work and a previously reported tagD mutant were not viable under phosphate-limiting conditions in the absence of complementation. Cell wall analysis of B. subtilis grown under phosphate-limited conditions showed that teichoic acid contributed approximately one-third of the wall anionic content. These data suggest that wall teichoic acid has an essential function in B. subtilis that cannot be replaced by teichuronic acid.

1969 ◽  
Vol 111 (1) ◽  
pp. 1-5 ◽  
Author(s):  
D C Ellwood ◽  
D. W. Tempest

1. Quantitative determination of the anionic polymers present in the walls of Bacillus subtilis var. niger organisms undergoing transition, in a chemostat culture, from either Mg2+-limitation to PO43−-limitation or K+-limitation to PO43−-limitation showed that teichuronic acid synthesis started immediately the culture became PO43−-limited and proceeded at a rate substantially faster than the rate of biomass synthesis. 2. Simultaneously, the cell-wall teichoic acid content diminished at a rate greater than that due to dilution by newly synthesized wall material, and fragments of teichoic acid and mucopeptide accumulated in the culture extracellular fluid. 3. Equally rapid reverse changes occurred when a PO43−-limited B. subtilis var. niger culture was returned to being Mg2+-limited. 4. It is concluded that in this organism both teichoic acid and teichuronic acid syntheses are expressions of a single genotype, and a mechanism for the control of synthesis of both polymers is suggested. 5. These results are discussed with reference to the constantly changing environmental conditions that obtain in a batch culture and the variation in bacterial cell-wall composition that is reported to occur throughout the growth cycle.


2008 ◽  
Vol 190 (14) ◽  
pp. 4989-4996 ◽  
Author(s):  
Catarina Baptista ◽  
Mário A. Santos ◽  
Carlos São-José

ABSTRACT Bacteriophage SPP1 targets the host cell membrane protein YueB to irreversibly adsorb and infect Bacillus subtilis. Interestingly, SPP1 still binds to the surface of yueB mutants, although in a completely reversible way. We evaluated here the relevance of a reversible step in SPP1 adsorption and identified the receptor(s) involved. We show that reversible adsorption is impaired in B. subtilis mutants defective in the glucosylation pathway of teichoic acids or displaying a modified chemical composition of these polymers. The results indicate that glucosylated poly(glycerolphosphate) cell wall teichoic acid is the major target for SPP1 reversible binding. Interaction with this polymer is characterized by a fast adsorption rate showing low-temperature dependence, followed by a rapid establishment of an equilibrium state between adsorbed and free phages. This equilibrium is basically determined by the rate of phage dissociation, which exhibits a strong dependence on temperature compatible with an Arrhenius law. This allowed us to determine an activation energy of 22.6 kcal/mol for phage release. Finally, we show that SPP1 reversible interaction strongly accelerates irreversible binding to YueB. Our results support a model in which fast SPP1 adsorption to and desorption from teichoic acids allows SPP1 to scan the bacterial surface for rapid YueB recognition.


2020 ◽  
Vol 11 (16) ◽  
pp. 4106-4118 ◽  
Author(s):  
Emily R. Caudill ◽  
Rodrigo Tapia Hernandez ◽  
Kyle P. Johnson ◽  
James T. O'Rourke ◽  
Lingchao Zhu ◽  
...  

Cationic gold nanoparticle interaction with strains of Bacillus subtilis is dictated by wall teichoic acid structure and composition.


Author(s):  
Jeanine Rismondo ◽  
Talal F. M. Haddad ◽  
Yang Shen ◽  
Martin J. Loessner ◽  
Angelika Gründling

ABSTRACTThe cell wall polymers wall teichoic acid (WTA) and lipoteichoic acid (LTA) are often modified with glycosyl and D-alanine residues. Recent studies have shown that a three-component glycosylation system is used for the modification of LTA in several Gram-positive bacteria including Bacillus subtilis and Listeria monocytogenes. In the L. monocytogenes 1/2a strain 10403S, the cytoplasmic glycosyltransferase GtlA is thought to use UDP-galactose to produce the C55-P-galactose lipid intermediate, which is transported across the membrane by an unknown flippase. Next, the galactose residue is transferred onto the LTA backbone on the outside of the cell by the glycosyltransferase GtlB. Here we show that GtcA is necessary for the glycosylation of LTA in L. monocytogenes 10403S and B. subtilis 168 and we hypothesize that these proteins act as C55-P-sugar flippases. With this we revealed that GtcA is involved in the glycosylation of both teichoic acid polymers in L. monocytogenes 10403S, namely WTA with N-acetylglucosamine and LTA with galactose residues. These findings indicate that the L. monocytogenes GtcA protein can act on different C55-P-sugar intermediates. Further characterization of GtcA in L. monocytogenes led to the identification of residues essential for its overall function as well as residues, which predominately impact WTA or LTA glycosylation.GRAPHICAL ABSTRACT


Microbiology ◽  
2006 ◽  
Vol 152 (6) ◽  
pp. 1709-1718 ◽  
Author(s):  
Pierre-Philippe Freymond ◽  
Vladimir Lazarevic ◽  
Blazenka Soldo ◽  
Dimitri Karamata

The ggaAB operon of Bacillus subtilis 168 encodes enzymes responsible for the synthesis of poly(glucosyl N-acetylgalactosamine 1-phosphate) [poly(GlcGalNAc 1-P)], a wall teichoic acid (WTA). Analysis of the nucleotide sequence revealed that both GgaA and GgaB contained the motif characteristic of sugar transferases, while GgaB was most likely to be bifunctional, being endowed with an additional motif present in glucosyl/glycerophosphate transferases. Transcription of the operon was thermosensitive, and took place from an unusually distant σ A-controlled promoter. The incorporation of the poly(GlcGalNAc 1-P) precursors by various mutants deficient in the synthesis of poly(glycerol phosphate), which is the most abundant WTA of strain 168, revealed that both WTAs were most likely to be attached to peptidoglycan (PG) through the same linkage unit (LU). The incorporation of poly(GlcGalNAc 1-P) precursors by protoplasts confirmed the existence of this LU, and provided further evidence that incorporation takes place at the outer surface of the protoplast membrane. The data presented here strengthen the view that biosynthesis of the LU, and the hooking of the LU-endowed polymer to PG, offer distinct widespread targets for antibiotics specific to Gram-positive bacteria.


mBio ◽  
2014 ◽  
Vol 5 (2) ◽  
Author(s):  
Volker Winstel ◽  
Patricia Sanchez-Carballo ◽  
Otto Holst ◽  
Guoqing Xia ◽  
Andreas Peschel

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 α-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 Φ187 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 Φ187 and enabled Φ187-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.


2015 ◽  
Vol 83 (11) ◽  
pp. 4247-4255 ◽  
Author(s):  
Jong-Ho Lee ◽  
Na-Hyang Kim ◽  
Volker Winstel ◽  
Kenji Kurokawa ◽  
Jesper Larsen ◽  
...  

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.


2015 ◽  
Vol 197 (8) ◽  
pp. 1492-1506 ◽  
Author(s):  
Letal I. Salzberg ◽  
Eric Botella ◽  
Karsten Hokamp ◽  
Haike Antelmann ◽  
Sandra Maaß ◽  
...  

ABSTRACTThe PhoPR two-component signal transduction system controls one of three responses activated byBacillus subtilisto adapt to phosphate-limiting conditions (PHO response). The response involves the production of enzymes and transporters that scavenge for phosphate in the environment and assimilate it into the cell. However, inB. subtilisand some otherFirmicutesbacteria, cell wall metabolism is also part of the PHO response due to the high phosphate content of the teichoic acids attached either to peptidoglycan (wall teichoic acid) or to the cytoplasmic membrane (lipoteichoic acid). Prompted by our observation that the phosphorylated WalR (WalR∼P) response regulator binds to more chromosomal loci than are revealed by transcriptome analysis, we established the PhoP∼P bindome in phosphate-limited cells. Here, we show that PhoP∼P binds to the chromosome at 25 loci: 12 are within the promoters of previously identified PhoPR regulon genes, while 13 are newly identified. We extend the role of PhoPR in cell wall metabolism showing that PhoP∼P binds to the promoters of four cell wall-associated operons (ggaAB,yqgS,wapA, anddacA), although none show PhoPR-dependent expression under the conditions of this study. We also show that positive autoregulation ofphoPRexpression and full induction of the PHO response upon phosphate limitation require PhoP∼P binding to the 3′ end of thephoPRoperon.IMPORTANCEThe PhoPR two-component system controls one of three responses mounted byB. subtilisto adapt to phosphate limitation (PHO response). Here, establishment of the phosphorylated PhoP (PhoP∼P) bindome enhances our understanding of the PHO response in two important ways. First, PhoPR plays a more extensive role in adaptation to phosphate-limiting conditions than was deduced from transcriptome analyses. Among 13 newly identified binding sites, 4 are cell wall associated (ggaAB,yqgS,wapA, anddacA), revealing that PhoPR has an extended involvement in cell wall metabolism. Second, amplification of the PHO response must occur by a novel mechanism since positive autoregulation ofphoPRexpression requires PhoP∼P binding to the 3′ end of the operon.


2009 ◽  
Vol 191 (13) ◽  
pp. 4482-4484 ◽  
Author(s):  
Thomas Kohler ◽  
Christopher Weidenmaier ◽  
Andreas Peschel

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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