Protection of the general stress response σ^S factor by the CrsR regulator allows a rapid and efficient adaptation of Shewanella oneidensis

To cope with environmental stresses, bacteria have evolved various strategies, including the general stress response (GSR). GSR is governed by an alternative transcriptional σ factor named σ^S (RpoS) that associates with RNA polymerase and controls the expression of numerous genes. Previously, we have reported that posttranslational regulation of σ^S in the aquatic bacterium Shewanella oneidensis involves the CrsR-CrsA partner-switching regulatory system, but the exact mechanism by which CrsR and CrsA control σ^S activity is not completely unveiled. Here, using a translational gene fusion, we show that CrsR sequesters and protects σ^S during the exponential growth phase and thus enables rapid gene activation by σ^S as soon as the cells enter early stationary phase. We further demonstrate by an in vitro approach that this protection is mediated by the anti-σ domain of CrsR. Structure-based alignments of CsrR orthologs and other anti-σ factors identified a CsrR-specific region characteristic of a new family of anti-σ factors. We found that CrsR is conserved in many aquatic proteobacteria, and most of the time it is associated with CrsA. In conclusion, our results suggest that CsrR-mediated protection of σ^S during exponential growth enables rapid adaptation of S. oneidensis to changing and stressful growth conditions, and this ability is probably widespread among aquatic proteobacteria.