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A sporulation-specific, sigF-dependent protein, SspA, affects septum positioning in Streptomyces coelicolor.

ABSTRACT: The RNA polymerase sigma factor SigF controls late development during sporulation in the filamentous bacterium Streptomyces coelicolor. The only known SigF-dependent gene identified so far, SCO5321, is found in the biosynthetic cluster encoding spore pigment synthesis. Here we identify the first direct target for SigF, the gene sspA, encoding a sporulation-specific protein. Bioinformatic analysis suggests that SspA is a secreted lipoprotein with two PepSY signature domains. The sspA deletion mutant exhibits irregular sporulation septation and altered spore shape, suggesting that SspA plays a role in septum formation and spore maturation. The fluorescent translational fusion protein SspA-mCherry localized first to septum sites, then subsequently around the surface of the spores. Both SspA protein and sspA transcription are absent from the sigF null mutant. Moreover, in vitro transcription assay confirmed that RNA polymerase holoenzyme containing SigF is sufficient for initiation of transcription from a single sspA promoter. In addition, in vivo and in vitro experiments showed that sspA is a direct target of BldD, which functions to repress sporulation genes, including whiG, ftsZ and ssgB, during vegetative growth, co-ordinating their expression during sporulation septation.

SUBMITTER: Tzanis A

PROVIDER: S-EPMC4282423 | biostudies-literature | 2014 Jan

REPOSITORIES: biostudies-literature

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A sporulation-specific, sigF-dependent protein, SspA, affects septum positioning in Streptomyces coelicolor.

Tzanis Angelos A Dalton Kate A KA Hesketh Andrew A den Hengst Chris D CD Buttner Mark J MJ Thibessard Annabelle A Kelemen Gabriella H GH

Molecular microbiology 20131219 2

The RNA polymerase sigma factor SigF controls late development during sporulation in the filamentous bacterium Streptomyces coelicolor. The only known SigF-dependent gene identified so far, SCO5321, is found in the biosynthetic cluster encoding spore pigment synthesis. Here we identify the first direct target for SigF, the gene sspA, encoding a sporulation-specific protein. Bioinformatic analysis suggests that SspA is a secreted lipoprotein with two PepSY signature domains. The sspA deletion mut ...[more]

PMID: 24261854

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Project description:BackgroundThe sporulation of aerial hyphae of Streptomyces coelicolor is a complex developmental process. Only a limited number of the genes involved in this intriguing morphological differentiation programme are known, including some key regulatory genes. The aim of this study was to expand our knowledge of the gene repertoire involved in S. coelicolor sporulation.ResultsWe report a DNA microarray-based investigation of developmentally controlled gene expression in S. coelicolor. By comparing global transcription patterns of the wild-type parent and two mutants lacking key regulators of aerial hyphal sporulation, we found a total of 114 genes that had significantly different expression in at least one of the two mutants compared to the wild-type during sporulation. A whiA mutant showed the largest effects on gene expression, while only a few genes were specifically affected by whiH mutation. Seven new sporulation loci were investigated in more detail with respect to expression patterns and mutant phenotypes. These included SCO7449-7451 that affect spore pigment biogenesis; SCO1773-1774 that encode an L-alanine dehydrogenase and a regulator-like protein and are required for maturation of spores; SCO3857 that encodes a protein highly similar to a nosiheptide resistance regulator and affects spore maturation; and four additional loci (SCO4421, SCO4157, SCO0934, SCO1195) that show developmental regulation but no overt mutant phenotype. Furthermore, we describe a new promoter-probe vector that takes advantage of the red fluorescent protein mCherry as a reporter of cell type-specific promoter activity.ConclusionAerial hyphal sporulation in S. coelicolor is a technically challenging process for global transcriptomic investigations since it occurs only as a small fraction of the colony biomass and is not highly synchronized. Here we show that by comparing a wild-type to mutants lacking regulators that are specifically affecting processes in aerial hypha, it is possible to identify previously unknown genes with important roles in sporulation. The transcriptomic data reported here should also serve as a basis for identification of further developmentally important genes in future functional studies.

Dataset Information

A sporulation-specific, sigF-dependent protein, SspA, affects septum positioning in Streptomyces coelicolor.

Publications

A sporulation-specific, sigF-dependent protein, SspA, affects septum positioning in Streptomyces coelicolor.

Similar Datasets

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