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ABC transporters required for export of wall teichoic acids do not discriminate between different main chain polymers.

ABSTRACT: The cell envelopes of Gram-positive bacteria comprise two major constituents, peptidoglycan and teichoic acids. Wall teichoic acids (WTAs) are anionic glycophosphate polymers that play important roles in bacterial cell growth, division, and pathogenesis. They are synthesized intracellularly and exported by an ABC transporter to the cell surface, where they are covalently attached to peptidoglycan. We address here the substrate specificity of WTA transporters by substituting the Bacillus subtilis homologue, TagGH(Bs), with the Staphylococcus aureus homologue, TarGH(Sa). These transporters export structurally different substrates in their indigenous organisms, but we show that TarGH(Sa) can substitute for the B. subtilis transporter. Hence, substrate specificity does not depend on the WTA main chain polymer structure but may be determined by the conserved diphospholipid-linked disaccharide portion of the WTA precursor. We also show that the complemented B. subtilis strain becomes susceptible to a S. aureus-specific antibiotic, demonstrating that the S. aureus WTA transporter is the sole target of this compound.

SUBMITTER: Schirner K

PROVIDER: S-EPMC3098905 | biostudies-literature | 2011 May

REPOSITORIES: biostudies-literature

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ABC transporters required for export of wall teichoic acids do not discriminate between different main chain polymers.

Schirner Kathrin K Stone Laura K LK Walker Suzanne S

ACS chemical biology 20110215 5

The cell envelopes of Gram-positive bacteria comprise two major constituents, peptidoglycan and teichoic acids. Wall teichoic acids (WTAs) are anionic glycophosphate polymers that play important roles in bacterial cell growth, division, and pathogenesis. They are synthesized intracellularly and exported by an ABC transporter to the cell surface, where they are covalently attached to peptidoglycan. We address here the substrate specificity of WTA transporters by substituting the Bacillus subtilis ...[more]

PMID: 21280653

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Project description:Rhizosphere colonization by plant growth-promoting rhizobacteria (PGPR) along plant roots facilitates the ability of PGPR to promote plant growth and health. Thus, an understanding of the molecular mechanisms of the root colonization process by plant-beneficial Bacillus strains is essential for the use of these strains in agriculture. Here, we observed that an sfp gene mutant of the plant growth-promoting rhizobacterium Bacillus velezensis SQR9 was unable to form normal biofilm architecture, and differential protein expression was observed by proteomic analysis. A minor wall teichoic acid (WTA) biosynthetic protein, GgaA, was decreased over 4-fold in the Δsfp mutant, and impairment of the ggaA gene postponed biofilm formation and decreased cucumber root colonization capabilities. In addition, we provide evidence that the major WTA biosynthetic enzyme GtaB is involved in both biofilm formation and root colonization. The deficiency in biofilm formation of the ΔgtaB mutant may be due to an absence of UDP-glucose, which is necessary for the synthesis of biofilm matrix exopolysaccharides (EPS). These observations provide insights into the root colonization process by a plant-beneficial Bacillus strain, which will help improve its application as a biofertilizer.IMPORTANCEBacillus velezensis is a Gram-positive plant-beneficial bacterium which is widely used in agriculture. Additionally, Bacillus spp. are some of the model organisms used in the study of biofilms, and as such, the molecular networks and regulation systems of biofilm formation are well characterized. However, the molecular processes involved in root colonization by plant-beneficial Bacillus strains remain largely unknown. Here, we showed that WTAs play important roles in the plant root colonization process. The loss of the gtaB gene affects the ability of B. velezensis SQR9 to sense plant polysaccharides, which are important environmental cues that trigger biofilm formation and colonization in the rhizosphere. This knowledge provides new insights into the Bacillus root colonization process and can help improve our understanding of plant-rhizobacterium interactions.

Project description:A major feature of the pathogenicity of Staphylococcus aureus is its ability to secrete cytolytic toxins. This process involves the translocation of the toxins from the cytoplasm through the bacterial membrane and the cell wall to the external environment. The process of their movement through the membrane is relatively well defined, involving both general and toxin-specific secretory systems. Movement of the toxins through the cell wall was considered to involve the passive diffusion of the proteins through the porous cell wall structures; however, recent work suggests that this is more complex, and here we demonstrate a role for the wall teichoic acids (WTA) in this process. Utilizing a genome-wide association approach, we identified a polymorphism in the locus encoding the WTA biosynthetic machinery as associated with the cytolytic activity of the bacteria. We verified this association using an isogenic mutant set and found that WTA are required for the release of several cytolytic toxins from the bacterial cells. We show that this effect is mediated by a change in the electrostatic charge across the cell envelope that results from the loss of WTA. As a major target for the development of novel therapeutics, it is important that we fully understand the entire process of cytolytic toxin production and release. These findings open up a new aspect to the process of toxin release by a major human pathogen while also demonstrating that clinical isolates can utilize WTA production to vary their cytotoxicity, thereby altering their pathogenic capabilities. IMPORTANCE The production and release of cytolytic toxins is a critical aspect for the pathogenicity of many bacterial pathogens. In this study, we demonstrate a role for wall teichoic acids, molecules that are anchored to the peptidoglycan of the bacterial cell wall, in the release of toxins from S. aureus cells into the extracellular environment. Our findings suggest that this effect is mediated by a gradient of electrostatic charge which the presence of the negatively charged WTA molecules create across the cell envelope. This work brings an entirely new aspect to our understanding of the cytotoxicity of S. aureus and demonstrates a further means by which this major human pathogen can adapt its pathogenic capabilities.

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ABC transporters required for export of wall teichoic acids do not discriminate between different main chain polymers.

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ABC transporters required for export of wall teichoic acids do not discriminate between different main chain polymers.

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