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The starvation-stress response of Salmonella enterica serovar Typhimurium requires ^E-, but not CpxR-regulated extracytoplasmic functions

Department of Biomedical Sciences, University of South Alabama, Mobile, AL 36688, USA¹
Department of Veterinary Pathology, Glasgow University Veterinary School, Glasgow G61 1QH, UK²

Author for correspondence: Michael P. Spector. Tel: +1 251 380 2688. Fax: +1 251 380 2711. e-mail: mspector{at}usouthal.edu

Starvation of Salmonella enterica serovar Typhimurium (S. Typhimurium) for an exogenous source of carbon and energy (C-starvation) induces the starvation-stress response (SSR). The SSR functions to (i) maintain viability during long-term C-starvation and (ii) generate cross-resistance to other environmental stresses. The SSR is, at least partially, under the control of the alternative sigma factor, ^S. It is hypothesized that C-starvation causes cell envelope stresses that could induce the ^E and/or Cpx regulons, both of which control extracytoplasmic functions and, thus, may play a role in the regulation of the SSR. In support of this hypothesis, Western blot analysis showed that the relative levels of ^E increased during C-starvation, peaking after approximately 72 h of C-starvation; in contrast, CpxR levels remained relatively constant from exponential phase up to 72 h of C-starvation. To determine if ^E, and thus the regulon it controls, is an essential component of the SSR, several mutant strains were compared for their abilities to survive long-term C-starvation and to develop C-starvation-induced (CSI) cross-resistances. An rpoE mutant strain was significantly impaired in both long-term C-starvation survival (LT-CSS) and in CSI cross-resistance to challenges with 20 mM H₂O₂ for 40 min, 55 °C for 16 min, pH 3·1 for 60 min and 870·2 USP U polymyxin B ml^-1 (PmB) for 60 min, to varying degrees. These results suggest that C-starvation can generate signals that induce the rpoE regulon and that one or more members of the ^E regulon are required for maximal SSR function. Furthermore, evidence suggests that the ^E and ^S regulons function through separate mechanisms in the SSR. In contrast, C-starvation does not appear to generate signals required for Cpx regulon induction which support the findings that it is not required for LT-CSS or cross-resistance to H₂O₂, pH 3·1 or PmB challenges. However, it was required to achieve maximal cross-resistance to 55 °C. Therefore, ^E is a key regulatory component of the SSR and represents an additional factor required for the SSR of Salmonella.

Keywords: rpoE, extracytoplasmic stress, sigma factors

Abbreviations: CRP, cAMP receptor protein; CSI, C-starvation-inducible/-induced; ECF, extracytoplasmic function; LT-CSS, long-term C-starvation survival; MS hiPCN, MOPS-buffered salts medium non-limiting in glucose, phosphate and nitrogen; MS loC, MOPS-buffered salts medium limiting for glucose (C-source); PmB, polymyxin B; S. Typhimurium, Salmonella enterica serovar Typhimurium; SSR, starvation-stress response

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