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Phosphorylated Spo0A is a master regulator of stationary phase development in the model bacterium  Bacillus subtilis , controlling the formation of spores, biofilms, and cells competent for transformation. We have monitored the rate of transcription of the  spo0A  gene during growth in sporulation medium using promoter fusions to firefly luciferase. This rate increases sharply during transient diauxie-like pauses in growth rate and then declines as growth resumes. In contrast, the rate of transcription of an rRNA gene decreases and increases in parallel with the growth rate, as expected for stable RNA synthesis. The growth pause-dependent bursts of  spo0A  transcription, which reflect the activity of the  spo0A  vegetative promoter, are largely independent of all known regulators of  spo0A  transcription. Evidence is offered in support of a “passive regulation” model in which RNA polymerase stops transcribing  rRNA  genes during growth pauses, thus becoming available for the transcription of  spo0A . We show that the bursts are followed by the production of phosphorylated Spo0A, and we propose that they represent initial responses to stress that bring the average cell closer to the thresholds for transition to bimodally expressed developmental responses. Measurement of the numbers of cells expressing a competence marker before and after the bursts supports this hypothesis. In the absence of ppGpp, the increase in  spo0A  transcription that accompanies the entrance to stationary phase is delayed and sporulation is markedly diminished. In spite of this, our data contradicts the hypothesis that sporulation is initiated when a ppGpp-induced depression of the GTP pool relieves repression by CodY. We suggest that, while the programmed induction of sporulation that occurs in stationary phase is apparently provoked by increased flux through the phosphorelay, bet-hedging stochastic transitions to at least competence are induced by bursts in transcription.

Fluctuations in spo0A Transcription Control Rare Developmental Transitions in Bacillus subtilis