s-Dependent carbon-starvation induction of pbpG (PBP 7) is required for the starvation-stress response in Salmonella enterica serovar Typhimurium

Carbon-energy source starvation is a commonly encountered stress that can influence the epidemiology and virulence of Salmonella enterica serovars. Salmonella responds to C-starvation by eliciting the starvation-stress response (SSR), which allows for long-term C-starvation survival and cross-resistance to other stresses. The stiC locus was identified as a C-starvation-inducible, as-dependent locus required for a maximal SSR. We report here that the stiC locus is an operon composed of the yohC (putative transport protein) and pbpG (penicillin-binding protein-7/8) genes. yohC pbpG transcription is initiated from a as-dependent C-starvation-inducible promoter upstream of yohC. Another (as-independent) promoter, upstream of pbpG, drives lower constitutive pbpG transcription, primarily during exponential phase. C-starvation-inducible pbpG expression was required for development of the SSR in 5 h, but not 24 h, C-starved cells; yohC was dispensable for the SSR. Furthermore, the yohC pbpG operon is induced within MDCK epithelial cells, but was not essential for oral virulence in BALB/c mice. Thus, PBP 7 is required for physiological changes, occurring within the first few hours of C-starvation, essential for the development of the SSR. Lack of PBP 7, however, can be compensated for by further physiological changes developed in 24 h C-starved cells. This supports the dynamic overlapping and distinct nature of resistance pathways within the Salmonella SSR.