Mutual interplay between ArcA and σE orchestrates envelope stress response in Shewanella oneidensis

To survive and thrive in harsh and ever-changing environments, intricate mechanisms have evolved for bacterial cells to monitor perturbations impacting the integrity of their envelope and to mount an appropriate response to contain or repair the damage. In this study, we report in Shewanella oneidensis a previously undescribed mechanism for the envelope defect resulting from the loss of Arc, a two-component transcriptional regulatory system crucial for respiration. We uncovered sigma(E), a master regulator establishing and maintaining the integrity of the cell envelope in gamma-proteobacteria, as the determining factor for the cell envelope defect of the arcA mutant. When ArcA is depleted, sigma(E) activity is compromised by enhanced production of anti-sigma(E) protein RseA. Surprisingly, S. oneidensis sigma(E) is not essential for viability, but becomes so in the absence of ArcA. Furthermore, we demonstrated that there is an interplay between these two regulators as arcA expression is affected by availability of sigma(E). Overall, our results underscore functional interplay of regulatory systems for envelope stress response: although each of the systems may respond to perturbation of particular components of the envelope, they are functionally intertwined, working together to form an interconnected safety net.