The Temperature-Regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigX

Abstract

Thermo-Regulation of the cmaX-cfrX-cmpX Operon IMPORTANCE Because temperature is one of the first physical signal that allows bacteria to distinguish a potential host from its environment, the response of P. aeruginosa has been more investigated in case of elevated rather than low temperature. Here, we show that the ECFσ SigX is an effector in the latter condition, which controls the transcription of the two members of an intriguing operon encoding the mechanosensitive channel CmpX and the hypothetical protein CfrX, while cmaX is under the control of AlgU. In addition, we show that SigX is activated following membrane structure alterations. More generally, we have identified temperature as a key environmental factor regulating antagonistically the expression and the activity of the two major cell wall stress response ECFσ in P. aeruginosa, suggesting that they are involved in specific but interconnected networks, in which the AlgU-dependent global transcriptional regulator AmrZ (alginate and motility regulator Z) could play a role by a mechanism that remains to be explored.

Activation of the Cell Wall Stress Response in Pseudomonas aeruginosa Infected by a Pf4 Phage Variant

“…For instance, the absence of the major porin OprF triggered increased sigX expression by about three-fold [33]. The exposure of P. aeruginosa to a cold-shock condition or to a valinomycin treatment resulted in increased sigX transcription by about two-and 7-fold, respectively [39]. Noticeably, the latter condition resulted in increased sigX expression at levels similar to the ones observed in response to Pf4* phage treatment.…”

“…These two conditions lead to a cell wall stress, during which SigX is activated, suggesting a direct or indirect link between SigX activity and pel expression. Noticeably, amrZ, the product of which positively regulates the expression of pel but not psl in P. aeruginosa PAO1 [74], was recently shown to be part of the SigX regulon [39]. The amrZ expression was slightly increased in response to Pf4* infection, which correlated with SigX expression and activity.…”

“…In addition, expression of the SigX targets cfrX, cmpX and fabY were increased by 23.3, 28.0 and 5.1-fold, respectively, in Pf4*-T condition (Figure 5A). Previous studies have reported inducing conditions of sigX expression [33,35,[37][38][39]41,43]. For instance, the absence of the major porin OprF triggered increased sigX expression by about three-fold [33].…”

“…Microorganisms 2020, 8, x FOR PEER REVIEW 12 of 21 aeruginosa PAO1 [74], was recently shown to be part of the SigX regulon [39]. The amrZ expression was slightly increased in response to Pf4* infection, which correlated with SigX expression and activity.…”

“…Expression of oprF is controlled by AlgU [34] and SigX [35,36], and a mutant lacking OprF shows increased expression and activity of SigX in addition to AlgU [33]. SigX is activated in response to hypo-osmolarity [35,37], high sucrose concentration [38], cold-shock condition or valinomycin treatment [39]. As SigX is involved in de novo fatty acid biosynthesis [40,41], SigX activity affects membrane homeostasis [37,42,43] and membrane fluidity [29,40,41].…”