Abstract
Sporulation in Bacillus subtilis involves two cells that follow separate but coordinately regulated developmental programs. Late in sporulation, the developing spore (the forespore) resides within a mother cell. The regulation of the forespore transcription factor σG that acts at this stage has remained enigmatic. σG activity requires eight mother-cell proteins encoded in the spoIIIA operon and the forespore protein SpoIIQ. Several of the SpoIIIA proteins share similarity with components of specialized secretion systems. One of them resembles a secretion ATPase and we demonstrate that the ATPase motifs are required for σG activity. We further show that the SpoIIIA proteins and SpoIIQ reside in a multimeric complex that spans the two membranes surrounding the forespore. Finally, we have discovered that these proteins are all required to maintain forespore integrity. In their absence, the forespore develops large invaginations and collapses. Importantly, maintenance of forespore integrity does not require σG. These results support a model in which the SpoIIIA-SpoIIQ proteins form a novel secretion apparatus that allows the mother cell to nurture the forespore, thereby maintaining forespore physiology and σG activity during spore maturation.
Highlights
How cells communicate with each other is a fundamental biological question relevant to the development of multi-cellular organisms, microbial pathogenesis and communities of microorganisms
Our data support a model in which a novel secretion system is assembled in the double membrane that encases the spore within the mother cell
Maintenance of forespore integrity does not require sG indicating that forespore collapse is not a result of the failure to activate sG. These results suggest that the block to sG activity in the SpoIIIA and SpoIIQ mutants is a manifestation of the failure to maintain forespore integrity
Summary
How cells communicate with each other is a fundamental biological question relevant to the development of multi-cellular organisms, microbial pathogenesis and communities of microorganisms. Upon the initiation of sporulation, the developing cell divides asymmetrically, generating two cells of unequal size and dissimilar fate: a small cell (the prospective spore), referred to as the forespore, and a large cell called the mother cell [1,2]. These two cells lie side by side, but shortly after polar division the mother cell membranes migrate around the forespore in a phagocytic-like process, generating a cell within a cell. Once the spore is fully mature, the mother cell lyses releasing it into the environment
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