Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli

Abstract

During the transition from post-exponential to stationary phase, Escherichia coli changes from the motile-planktonic to the adhesive-sedentary “lifestyle.” We demonstrate this transition to be controlled by mutual inhibition of the FlhDC/motility and σ^S/adhesion control cascades at two distinct hierarchical levels. At the top level, motility gene expression and the general stress response are inversely coordinated by σ⁷⁰/σ^FliA/σ^S competition for core RNA polymerase and the FlhDC-controlled FliZ protein acting as a σ^S inhibitor. At a lower level, the signaling molecule bis-(3′–5′)-cyclic-diguanosine monophosphate (c-di-GMP) reduces flagellar activity and stimulates transcription of csgD, which encodes an essential activator of adhesive curli fimbriae expression. This c-di-GMP is antagonistically controlled by σ^S-regulated GGDEF proteins (mainly YegE) and YhjH, an EAL protein and c-di-GMP phosphodiesterase under FlhDC/FliA control. The switch from motility-based foraging to the general stress response and curli expression requires σ^S-modulated down-regulation of expression of the flagellar regulatory cascade as well as proteolysis of the flagellar master regulator FlhDC. Control of YhjH by FlhDC and of YegE by σ^S produces a fine-tuned checkpoint system that “unlocks” curli expression only after down-regulation of flagellar gene expression. In summary, these data reveal the logic and sequence of molecular events underlying the motile-to-adhesive “lifestyle” switch in E. coli.