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,...
