A Quality-Control Mechanism Removes Unfit Cells from a Population of Sporulating Bacteria

• During sporulation, misassembly of the spore envelope causes CmpA-mediated lysis
• CmpA is a ClpXP adaptor for degradation of the morphogenetic protein SpoIVA
• The CmpA pathway helps to ensure evolutionary maintenance of the sporulation program

SummaryRecent discoveries of regulated cell death in bacteria have led to speculation about possible benefits that apoptosis-like pathways may confer to single-celled organisms. However, establishing how these pathways provide increased ecological fitness has remained difficult to determine. Here, we report a pathway in Bacillus subtilis in which regulated cell death maintains the fidelity of sporulation through selective removal of cells that misassemble the spore envelope. The spore envelope, which protects the dormant spore’s genome from environmental insults, uses the protein SpoIVA as a scaffold for assembly. We found that disrupting envelope assembly activates a cell death pathway wherein the small protein CmpA acts as an adaptor to the AAA+ ClpXP protease to degrade SpoIVA, thereby halting sporulation and resulting in lysis of defective sporulating cells. We propose that removal of unfit cells from a population of terminally differentiating cells protects against evolutionary deterioration and ultimately loss of the sporulation program.

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