Dataset Information

Hyphal compartmentalization and sporulation in Streptomyces require the conserved cell division protein SepX.

ABSTRACT: Filamentous actinobacteria such as Streptomyces undergo two distinct modes of cell division, leading to partitioning of growing hyphae into multicellular compartments via cross-walls, and to septation and release of unicellular spores. Specific determinants for cross-wall formation and the importance of hyphal compartmentalization for Streptomyces development are largely unknown. Here we show that SepX, an actinobacterial-specific protein, is crucial for both cell division modes in Streptomyces venezuelae. Importantly, we find that sepX-deficient mutants grow without cross-walls and that this substantially impairs the fitness of colonies and the coordinated progression through the developmental life cycle. Protein interaction studies and live-cell imaging suggest that SepX contributes to the stabilization of the divisome, a mechanism that also requires the dynamin-like protein DynB. Thus, our work identifies an important determinant for cell division in Streptomyces that is required for cellular development and sporulation.

SUBMITTER: Bush MJ

PROVIDER: S-EPMC8748795 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Hyphal compartmentalization and sporulation in Streptomyces require the conserved cell division protein SepX.

Bush Matthew J MJ Gallagher Kelley A KA Chandra Govind G Findlay Kim C KC Schlimpert Susan S

Nature communications 20220110 1

Filamentous actinobacteria such as Streptomyces undergo two distinct modes of cell division, leading to partitioning of growing hyphae into multicellular compartments via cross-walls, and to septation and release of unicellular spores. Specific determinants for cross-wall formation and the importance of hyphal compartmentalization for Streptomyces development are largely unknown. Here we show that SepX, an actinobacterial-specific protein, is crucial for both cell division modes in Streptomyces ...[more]

PMID: 35013186

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Project description:UnlabelledWhiA is a highly unusual transcriptional regulator related to a family of eukaryotic homing endonucleases. WhiA is required for sporulation in the filamentous bacterium Streptomyces, but WhiA homologues of unknown function are also found throughout the Gram-positive bacteria. To better understand the role of WhiA in Streptomyces development and its function as a transcription factor, we identified the WhiA regulon through a combination of chromatin immunoprecipitation-sequencing (ChIP-seq) and microarray transcriptional profiling, exploiting a new model organism for the genus, Streptomyces venezuelae, which sporulates in liquid culture. The regulon encompasses ~240 transcription units, and WhiA appears to function almost equally as an activator and as a repressor. Bioinformatic analysis of the upstream regions of the complete regulon, combined with DNase I footprinting, identified a short but highly conserved asymmetric sequence, GACAC, associated with the majority of WhiA targets. Construction of a null mutant showed that whiA is required for the initiation of sporulation septation and chromosome segregation in S. venezuelae, and several genes encoding key proteins of the Streptomyces cell division machinery, such as ftsZ, ftsW, and ftsK, were found to be directly activated by WhiA during development. Several other genes encoding proteins with important roles in development were also identified as WhiA targets, including the sporulation-specific sigma factor σ(WhiG) and the diguanylate cyclase CdgB. Cell division is tightly coordinated with the orderly arrest of apical growth in the sporogenic cell, and filP, encoding a key component of the polarisome that directs apical growth, is a direct target for WhiA-mediated repression during sporulation.ImportanceSince the initial identification of the genetic loci required for Streptomyces development, all of the bld and whi developmental master regulators have been cloned and characterized, and significant progress has been made toward understanding the cell biological processes that drive morphogenesis. A major challenge now is to connect the cell biological processes and the developmental master regulators by dissecting the regulatory networks that link the two. Studies of these regulatory networks have been greatly facilitated by the recent introduction of Streptomyces venezuelae as a new model system for the genus, a species that sporulates in liquid culture. Taking advantage of S. venezuelae, we have characterized the regulon of genes directly under the control of one of these master regulators, WhiA. Our results implicate WhiA in the direct regulation of key steps in sporulation, including the cessation of aerial growth, the initiation of cell division, and chromosome segregation.

Project description:The cell wall of monoderm bacteria consists of peptidoglycan and glycopolymers in roughly equal proportions and is crucial for cellular integrity, cell shape, and bacterial vitality. Despite the immense value of Streptomyces in biotechnology and medicine as antibiotic producers, we know very little about their cell wall biogenesis, composition, and functions. Here, we have identified the LCP-LytR_C domain protein CglA (Vnz_13690) as a key glycopolymer ligase, which specifically localizes in zones of cell wall biosynthesis in S. venezuelae. Reduced amount of glycopolymers in the cglA mutant results in enlarged vegetative hyphae and failures in FtsZ-rings formation and positioning. Consequently, division septa are misplaced leading to the formation of aberrant cell compartments, misshaped spores, and reduced cell vitality. In addition, we report our discovery that c-di-AMP signaling and decoration of the cell wall with glycopolymers are physiologically linked in Streptomyces since the deletion of cglA restores growth of the S. venezuelae disA mutant at high salt. Altogether, we have identified and characterized CglA as a novel component of cell wall biogenesis in Streptomyces, which is required for cell shape maintenance and cellular vitality in filamentous, multicellular bacteria.IMPORTANCEStreptomyces are our key producers of antibitiotics and other bioactive molecules and are, therefore, of high value for medicine and biotechnology. They proliferate by apical extension and branching of hyphae and undergo complex cell differentiation from filaments to spores during their life cycle. For both, growth and sporulation, coordinated cell wall biogenesis is crucial. However, our knowledge about cell wall biosynthesis, functions, and architecture in Streptomyces and in other Actinomycetota is still very limited. Here, we identify CglA as the key enzyme needed for the attachment of glycopolymers to the cell wall of S. venezuelae. We demonstrate that defects in the cell wall glycopolymer content result in loss of cell shape in these filamentous bacteria and show that division-competent FtsZ-rings cannot assemble properly and fail to be positioned correctly. As a consequence, cell septa placement is disturbed leading to the formation of misshaped spores with reduced viability.

Dataset Information

Hyphal compartmentalization and sporulation in Streptomyces require the conserved cell division protein SepX.

Publications

Hyphal compartmentalization and sporulation in Streptomyces require the conserved cell division protein SepX.

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