A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of sigmaS (RpoS) in E. coli.

The general stress sigma factor sigma(S) (RpoS) in Escherichia coli is controlled at the levels of transcription, translation, and proteolysis. Here we demonstrate that the phosphorylated response regulator ArcA is a direct repressor of rpoS transcription that binds to two sites flanking the major rpoS promoter, with the upstream site overlapping an activating cAMP-CRP-binding site. The histidine sensor kinase ArcB not only phosphorylates ArcA, but also the sigma(S) proteolytic targeting factor RssB, and thereby stimulates sigma(S) proteolysis. Thus, ArcB/ArcA/RssB constitute a branched "three-component system", which coordinates rpoS transcription and sigma(S) proteolysis and thereby maintains low sigma(S) levels in rapidly growing cells. We suggest that the redox state of the quinones, which controls autophosphorylation of ArcB, not only monitors oxygen but also energy supply, and we show that the ArcB/ArcA/RssB system is involved in sigma(S) induction during entry into starvation conditions. Moreover, this induction is enhanced by a positive feedback that involves sigma(S)-dependent induction of ArcA, which further reduces sigma(S) proteolysis, probably by competing with RssB for residual phosphorylation by ArcB.