Abstract

Members of the family of SsgA-like proteins (SALPs) are found exclusively in sporulating actinomycetes, and SsgA itself activates sporulation-specific cell division. We previously showed that SALPs play a chaperonin-like role in supporting the function of enzymes involved in peptidoglycan maintenance (PBPs and autolysins). Here we show that SsgA localizes dynamically during development, and most likely marks the sites where changes in local cell-wall morphogenesis are required, in particular septum formation and germination. In sporogenic aerial hyphae, SsgA initially localizes as strong foci to the growing tips, followed by distribution as closely spaced foci in a pattern similar to an early stage of FtsZ assembly. Spore septa formed in these hyphae colocalize with single SsgA-GFP foci, and when the maturing spores are separated, these foci are distributed symmetrically, resulting in two foci per mature spore. Evidence is provided that SsgA also controls the correct localization of germination sites. Transcriptome analysis revealed that expression of around 300 genes was significantly altered in mutants in ssgA and its regulatory gene ssgR. The list includes surprisingly many known developmental genes, most of which were upregulated, highlighting SsgA as a key player in the control of Streptomyces development.

Highlights

  • The correct timing and localization of cell division, which involves dynamic reorganization of cell-wall synthesis and breakdown, are among the most studied topics in modern microbial cell biology

  • Multiple septa are simultaneously synthesized in a process in which proteins required for the formation of bacterial divisomes are presumably sequentially directed to the Z ring (Bramhill, 1997; Errington et al, 2003)

  • We showed previously that ssgA mutants produce aerial mycelium but have a conditional non-sporulating phenotype, failing to sporulate on glucose-containing solid media, while some spores are produced on mannitolcontaining media

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Summary

Introduction

The correct timing and localization of cell division, which involves dynamic reorganization of cell-wall synthesis and breakdown, are among the most studied topics in modern microbial cell biology. In most bacteria a single septum forms the cleavage furrow dividing the mother cell into daughter cells, but during growth of the Gram-positive mycelial bacterium Streptomyces, vegetative hyphae are divided only occasionally by vegetative septa or cross walls, giving multigenomic compartments, while reproduction involves the simultaneous production of many specialized septa to form long chains of unigenomic spores from multigenomic aerial hyphal compartments (Wildermuth and Hopwood, 1970; McCormick et al, 1994; Flärdh et al, 2000). In contrast to vegetative crosswalls, multiple sporulation septa are produced simultaneously and in a highly co-ordinated way within a sporogenic aerial hypha. The segregation of DNA into the prespore compartments is partially dependent on ParA and ParB (Jakimowicz et al, 2002a; 2005), is accompanied by DNA condensation, and appears to be completed by a process involving septum-located FtsK (Wang et al, 2007). Much remains to be learned about the co-ordinated production of up to 100 sporulation septa in aerial hyphae

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