Shifts from glucose to certain secondary carbon-sources result in activation of the extracytoplasmic function sigma factor σ E in Salmonella enterica serovar Typhimurium
Authors: Kenyon William J. , Thomas Sheena M. , Johnson Erin , Pallen Mark J. , Spector Michael P. 
Published: July 2005

Salmonella entericaserovar Typhimurium (S. Typhimurium) elicits the starvation-stress response (SSR) due to starvation for an essential nutrient, e.g. a carbon/energy source (C-source). As part of the SSR, the alternative sigma factorσEis activated and induced. The authors suspect that this activation is, in part, triggered by changes in theS. Typhimurium cell envelope occurring during the adaptation from growth to carbon/energy starvation (C-starvation), and resulting in an increased need forσE-regulated factors involved in the proper folding and assembly of newly synthesized proteins destined for this extracytoplasmic compartment. This led to the hypothesis that aσEactivation signal might arise during C-source shifts that cause the induction of proteins localized to the extracytoplasmic compartment, i.e. the outer membrane or periplasm, of the cell. To test this hypothesis, cultures were grown in minimal medium containing enough glucose to reach mid-exponential-phase, plus a non-limiting amount of a secondary ‘less-preferred’ but utilizable carbon/energy source. TheσEactivity was then monitored using plasmids carryingrpoEP1– andrpoEP2–lacZtranscriptional fusions, which exhibitσE-independent and -dependentlacZexpression, respectively. The secondary C-sources maltose, succinate and citrate, which have extracytoplasmic components involved in their utilization (e.g. LamB), resulted in a discernible diauxic lag period and a sustained increase inσEactivity. Growth transition from glucose to other utilizable phosphotransferase (PTS) and non-PTS C-sources, such as trehalose, mannose, mannitol, fructose, glycerol,d-galactose orl-arabinose, did not cause a discernible diauxic lag period or a sustained increase inσEactivity. Interestingly, a shift from glucose to melibiose, which does not use an extracytoplasmic-localized protein for uptake, did cause an observable diauxic lag period but did not result in a sustained increase inσEactivity. In addition, overexpression of LamB from an arabinose-inducible promoter leads to a significant increase inσEactivity in the absence of a glucose to maltose shift or C-starvation. Furthermore, a ΔlamB : : Ω-Kmrmutant, lacking the LamB maltoporin, exhibited an approximately twofold reduction in the sustainedσEactivity observed during a glucose to maltose shift, again supporting the hypothesis. Interestingly, the LamB protein lacks the typical Y-X-F terminal tripeptide of the OmpC-like peptides that activate DegS protease activity leading toσEactivation. It does, however, possess a terminal pentapeptide (Q-M-E-I-W-W) that may function as a ligand for a putative class II PDZ-binding site. The authors therefore propose that theσEregulon ofS. Typhimurium not only is induced in response to deleterious environmental conditions, but also plays a role in the adaptation of cells to new growth conditions that necessitate changes in the extracytoplasmic compartment of the cell, which may involve alternative signal recognition and activation pathways that are independent of DegS.