Genetic Analysis of
            <i>SCO2997</i>
            , Encoding a TagF Homologue, Indicates a Role for Wall Teichoic Acids in Sporulation of Streptomyces coelicolor A3(2)

Kleinschnitz, Eva-Maria; Latus, Annette; Sigle, Steffen; Maldener, Iris; Wohlleben, Wolfgang; Muth, Günther

doi:10.1128/jb.05782-11

Cited by 18 publications

(11 citation statements)

References 39 publications

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“…Extensive protein interactions have been detected within the complex, and they also extend to the S. coelicolor homologs of RodZ and FtsI, as well as two additional penicillin-binding proteins (Kleinschnitz et al, 2011b). Further interaction partners and possible members of the SSSC complex were found by a two-hybrid screen, including a membrane protein encoded by an interesting gene cluster (cmdABCDEF) required for normal sporulation (Xie et al, 2009;Kleinschnitz et al, 2011b), and another membrane protein (SCO2584) that may be related to wall teichoic acid biosynthesis, which was recently reported to be required for normal spore wall assembly (Kleinschnitz et al, 2011a).…”

Section: Chromosome Segregationmentioning

confidence: 99%

Signals and regulators that governStreptomycesdevelopment

2012

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Streptomyces coelicolor is the genetically best characterized species of a populous genus belonging to the Gram-positive Actinobacteria. Streptomycetes are filamentous soil organisms, well known for the production of a plethora of biologically active secondary metabolic compounds. The Streptomyces developmental life cycle is uniquely complex, and involves coordinated multicellular development with both physiological and morphological differentiation of several cell types, culminating in production of secondary metabolites and dispersal of mature spores. This review presents a current appreciation of the signaling mechanisms used to orchestrate the decision to undergo morphological differentiation, and the regulators and regulatory networks that direct the intriguing development of multigenomic hyphae, first to form specialized aerial hyphae, and then to convert them into chains of dormant spores. This current view of S. coelicolor development is destined for rapid evolution as data from “-omics” studies shed light on gene regulatory networks, new genetic screens identify hitherto unknown players, and the resolution of our insights into the underlying cell biological processes steadily improve.

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Section: Chromosome Segregationmentioning

confidence: 99%

Signals and regulators that governStreptomycesdevelopment

2012

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“…A set of genes, tentatively encoding enzymes for teichuronic acid biosynthesis, 27 are activated by PhoP following phosphate starvation and contain PhoP-binding sites in their promoter regions, and some genes, presumably involved in teichoic acid biosynthesis, are repressed by phosphate depletion. 4,19 Genes for iron metabolism and oxidative stress In several bacteria, it is well known that phosphate limitation triggers oxidative stress.…”

Section: Genetic Basis Of Phosphate Control Of Metabolismmentioning

confidence: 99%

The master regulator PhoP coordinates phosphate and nitrogen metabolism, respiration, cell differentiation and antibiotic biosynthesis: comparison in Streptomyces coelicolor and Streptomyces avermitilis

2017

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Phosphate limitation is important for production of antibiotics and other secondary metabolites in Streptomyces. Phosphate control is mediated by the two-component system PhoR-PhoP. Following phosphate depletion, PhoP stimulates expression of genes involved in scavenging, transport and mobilization of phosphate, and represses the utilization of nitrogen sources. PhoP reduces expression of genes for aerobic respiration and activates nitrate respiration genes. PhoP activates genes for teichuronic acid formation and reduces expression of genes for phosphate-rich teichoic acid biosynthesis. In Streptomyces coelicolor, PhoP repressed several differentiation and pleiotropic regulatory genes, which affects development and indirectly antibiotic biosynthesis. A new bioinformatics analysis of the putative PhoP-binding sequences in Streptomyces avermitilis was made. Many sequences in S. avermitilis genome showed high weight values and were classified according to the available genetic information. These genes encode phosphate scavenging proteins, phosphate transporters and nitrogen metabolism genes. Among of the genes highlighted in the new studies was aveR, located in the avermectin gene cluster, encoding a LAL-type regulator, and afsS, which is regulated by PhoP and AfsR. The sequence logo for S. avermitilis PHO boxes is similar to that of S. coelicolor, with differences in the weight value for specific nucleotides in the sequence. INTRODUCTIONPhosphate is one of the essential nutrients of all living beings. In early studies, Martín and Demain 1 reported that, following phosphate starvation, there is a change in the metabolism of the antibiotic producing strains, which causes the slowdown of primary metabolism and triggers production of secondary metabolites. This early hypothesis has been largely confirmed by the research developed in the last few decades and is discussed in more detail below taking into account recent developments in the coordination of secondary metabolism. The aim of this article is to present an up-to-date integrative view of the PhoP regulation of metabolism in Streptomyces.

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“…Whereas B. subtilis contains three LCP transferases (10), S. coelicolor M145 encodes 11 LCPs, which fall into two groups defined by the presence of the C-terminal LytR_C domain of unknown catalytic function ( Table 2). The TagV-like PdtA (SCO2578) is encoded as part of a putative gene cluster involved in anionic glycopolymer synthesis (26) and was previously identified in a screen of a genomic library as an interaction partner of several SSSC proteins, suggesting a role in sporulation (23). Despite the presence of 10 further homologs, the deletion of pdtA caused a severe phenotype.…”

Section: Discussionmentioning

confidence: 99%

“…pdtA is probably cotranscribed with the nicotinate-nucleotide adenylyltransferase gene SCO2579 (Fig. 1A) and lies close to other putative anionic glycopolymer-related genes (26).…”

Section: Resultsmentioning

confidence: 99%

“…Streptomyces coelicolor A3(2) encodes several homologues of Tag proteins (26) directing WTA synthesis in B. subtilis, although the major glycopolymer of S. coelicolor has been recently characterized as teichulosonic acid. The S. coelicolor teichulosonic acid is a phosphate-free polymer of up to seven repeating units composed of galactose (Gal) and the neuraminic acid-related 2-keto-3-deoxy-D-glycero-D-galacto-nononic acid (Kdn), often substituted with GlcNAc or a methyl group.…”

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Polydiglycosylphosphate Transferase PdtA (SCO2578) of Streptomyces coelicolor A3(2) Is Crucial for Proper Sporulation and Apical Tip Extension under Stress Conditions

Sigle

Steblau

Wohlleben

et al. 2016

Appl Environ Microbiol

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Although anionic glycopolymers are crucial components of the Gram-positive cell envelope, the relevance of anionic glycopolymers for vegetative growth and morphological differentiation of Streptomyces coelicolor A3(2) is unknown. Here, we show that the LytR-CpsA-Psr (LCP) protein PdtA (SCO2578), a TagV-like glycopolymer transferase, has a dual function in the S. coelicolor A3(2) life cycle. Despite the presence of 10 additional LCP homologs, PdtA is crucial for proper sporulation. The integrity of the spore envelope was severely affected in a pdtA deletion mutant, resulting in 34% nonviable spores. pdtA deletion caused a significant reduction in the polydiglycosylphosphate content of the spore envelope. Beyond that, apical tip extension and normal branching of vegetative mycelium were severely impaired on high-salt medium. This growth defect coincided with the mislocalization of peptidoglycan synthesis. Thus, PdtA itself or the polydiglycosylphosphate attached to the peptidoglycan by the glycopolymer transferase PdtA also has a crucial function in apical tip extension of vegetative hyphae under stress conditions. IMPORTANCEAnionic glycopolymers are underappreciated components of the Gram-positive cell envelope. They provide rigidity to the cell wall and position extracellular enzymes involved in peptidoglycan remodeling. Although Streptomyces coelicolor A3(2), the model organism for bacterial antibiotic production, is known to produce two distinct cell wall-linked glycopolymers, teichulosonic acid and polydiglycosylphosphate, the role of these glycopolymers in the S. coelicolor A3(2) life cycle has not been addressed so far. This study reveals a crucial function of the anionic glycopolymer polydiglycosylphosphate for the growth and morphological differentiation of S. coelicolor A3(2). Polydiglycosylphosphate is attached to the spore wall by the LytR-CpsA-Psr protein PdtA (SCO2578), a component of the Streptomyces spore wall-synthesizing complex (SSSC), to ensure the integrity of the spore envelope. Surprisingly, PdtA also has a crucial role in vegetative growth under stress conditions and is required for proper peptidoglycan incorporation during apical tip extension. The bacterial cell envelope forms a protective shield around bacteria, providing mechanical strength and conferring cell shape and size (1). The cell envelope is the interface for the interaction with the environment and one of the most important targets of antibiotics. The cell envelope of Gram-positive bacteria consists of a multilayered peptidoglycan (PG), a heteropolymer of peptide cross-linked glycan strands, membrane-anchored lipoteichoic acids, PG-bound wall teichoic acids (WTA), exopolysaccharides, and surface proteins (2, 3). WTAs, which can account for about 60% of the total mass of the cell envelope (4), are carbohydrate-based anionic glycopolymers often substituted with D-alanine ester residues, giving the molecule zwitterionic properties. They provide rigidity to the cell wall by attracting cations, such as magnesium and sodium,...

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Genetic Analysis of SCO2997 , Encoding a TagF Homologue, Indicates a Role for Wall Teichoic Acids in Sporulation of Streptomyces coelicolor A3(2)

Cited by 18 publications

References 39 publications

Signals and regulators that governStreptomycesdevelopment

Signals and regulators that governStreptomycesdevelopment

The master regulator PhoP coordinates phosphate and nitrogen metabolism, respiration, cell differentiation and antibiotic biosynthesis: comparison in Streptomyces coelicolor and Streptomyces avermitilis

Polydiglycosylphosphate Transferase PdtA (SCO2578) of Streptomyces coelicolor A3(2) Is Crucial for Proper Sporulation and Apical Tip Extension under Stress Conditions

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