Global Analysis of Extracytoplasmic Stress Signaling in Escherichia coli

Abstract

The Bae, Cpx, Psp, Rcs, and σ ^E pathways constitute the Escherichia coli signaling systems that detect and respond to alterations of the bacterial envelope. Contributions of these systems to stress response have previously been examined individually; however, the possible interconnections between these pathways are unknown. Here we investigate the dynamics between the five stress response pathways by determining the specificities of each system with respect to signal-inducing conditions, and monitoring global transcriptional changes in response to transient overexpression of each of the effectors. Our studies show that different extracytoplasmic stress conditions elicit a combined response of these pathways. Involvement of the five pathways in the various tested stress conditions is explained by our unexpected finding that transcriptional responses induced by the individual systems show little overlap. The extracytoplasmic stress signaling pathways in E. coli thus regulate mainly complementary functions whose discrete contributions are integrated to mount the full adaptive response.

Author Summary

Bacteria possess various signaling systems that sense and respond to environmental conditions. The bacterial envelope is at the front line for most external stress conditions; its components sense perturbations and transmit signals to induce transcriptional reprogramming, leading to an adaptive response. In Escherichia coli, at least five response pathways, called Bae, Cpx, Psp, Rcs, and σ ^E, are induced in response to envelope stress. To date, these pathways have been studied mainly individually, and the interconnections and/or overlaps between them have not been extensively characterized. The present study establishes two important characteristics of stress response in E. coli: first, that a given stress solicits the combined responses of several pathways; second, that each individual pathway controls a discrete set of genes involved in the response, and shows little overlap with other pathways. Based on previous knowledge and the present data, we propose that an environmental stress probably impacts on the cell envelope by inducing numerous alterations, each of which may be perceived by different pathways of the stress response and contributes to adapting the cell to different aspects of the stress damage. The extracytoplasmic stress signaling pathways in E. coli thus regulate mainly complementary functions whose discrete contributions are integrated to mount the full adaptive response.