Degradation of the general stress sigma factor sigmaS of Escherichia coli is a prime example of regulated proteolysis in prokaryotes. Whereas exponentially growing cells rapidly degrade sigmaS, various stress conditions result in stabilization and, therefore, rapid accumulation of sigmaS. Proteolysis of sigmaS requires the response regulator RssB, a direct recognition factor with phosphorylation-dependent affinity for sigmaS, which targets sigmaS to the ClpXP protease. Here, we demonstrate that a sudden increase in sigmaS synthesis results in sigmaS stabilization, indicating titration of an essential proteolytic component. Evidence is provided that RssB is the overall rate-limiting factor for sigmaS proteolysis. As a consequence, the cell has to continuously adjust the expression of RssB to sigmaS in order to maintain sigmaS proteolysis in growing cells, despite variations in the rate of sigmaS synthesis. Such homeostatic feedback-coupling is provided by rssB transcription being dependent on the sigmaS-controlled rssAB operon promoter. However, strong and rapid increases in sigmaS synthesis, in re-sponse to acute stress, exceed the compensatory potential of this feedback loop with the result that sigmaS is stabilized because of RssB titration. We propose that RssB control of sigmaS proteolysis functions as a genetic switch, in which (i) the 'off' state (low sigmaS levels caused by proteolysis) is stabilized by a homeostatic negative feedback, and (ii) the threshold for switching to the 'on' state (high levels of stable sigmaS) is dependent on the cellular level of active, i.e. phosphorylated RssB.