Extracytoplasmic function sigma factors in Pseudomonas aeruginosa

Chevalier, Sylvie; Bouffartigues, Emeline; Bazire, Alexis; Tahrioui, Ali; Duchesne, Rachel; Tortuel, Damien; Maillot, Olivier; Clamens, Thomas; Orange, Nicole; Feuilloley, Marc; Lesouhaitier, Olivier; Dufour, Alain; Cornélis, Pierre

doi:10.1016/j.bbagrm.2018.04.008

Cited by 72 publications

(81 citation statements)

References 235 publications

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“…This included many AlgU-regulated and stress-related proteins, the expression of which could be explained by the activation of AlgU in both strains, but also several other proteins, such as pyoverdine synthesis and type VI secretion system proteins. Analogously to AlgU regulon genes, the pyoverdine genes in P. aeruginosa are controlled by extracytoplasmic-function (ECF) sigma factors such as PvdS, FpvI, and SigX (45,46). Given that activation of ECF sigma factors depends on transmembrane signaling, the upregulation of pyoverdine synthesis proteins may result from membrane stress as well.…”

Section: Discussionmentioning

confidence: 99%

The TonB_m-PocAB System Is Required for Maintenance of Membrane Integrity and Polar Position of Flagella in Pseudomonas putida

et al. 2019

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TonB-ExbB-ExbD-like energy transduction systems are widespread among Gram-negative bacteria. While most species have only one copy of tonB-exbBD genes, the Pseudomonas species possess more TonB-ExbBD homologues. One of them, the TonB3-PocA-PocB complex, was recently shown to be required for polar localization of FlhF and, thus, the flagella in Pseudomonas aeruginosa. Here, we show that the orthologous TonBm-PocA-PocB complex is important for polar localization of FlhF and flagella in Pseudomonas putida as well. Additionally, the system is necessary for maintaining membrane integrity, as the inactivation of the TonBm-PocAB complex results in increased membrane permeability, lowered stress tolerance, and conditional cell lysis. Interestingly, the functionality of TonBm-PocAB complex is more important for stationary than for exponentially growing bacteria. The whole-cell proteome analysis provided a likely explanation for this growth phase dependence, as extensive reprogramming was disclosed in an exponentially growing tonBm deletion strain, while only a few proteomic changes, mostly downregulation of outer membrane proteins, were determined in the stationary-phase ΔtonBm strain. We propose that this response in exponential phase, involving, inter alia, activation of AlgU and ColR regulons, can compensate for TonBm-PocAB’s deficiency, while stationary-phase cells are unable to alleviate the lack of TonBm-PocAB. Our results suggest that mislocalization of flagella does not cause the membrane integrity problems; rather, the impaired membrane intactness of the TonBm-PocAB-deficient strain could be the reason for the random placement of flagella. IMPORTANCE The ubiquitous Pseudomonas species are well adapted to survive in a wide variety of environments. Their success relies on their versatile metabolic, signaling, and transport ability but also on their high intrinsic tolerance to various stress factors. This is why the study of the stress-surviving mechanisms of Pseudomonas species is of utmost importance. The stress tolerance of Pseudomonads is mainly achieved through the high barrier property of their membranes. Here, we present evidence that the TonB-ExbBD-like TonBm-PocAB system is involved in maintaining the membrane homeostasis of Pseudomonas putida, and its deficiency leads to lowered stress tolerance and conditional cell lysis.

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Section: Discussionmentioning

confidence: 99%

The TonB_m-PocAB System Is Required for Maintenance of Membrane Integrity and Polar Position of Flagella in Pseudomonas putida

et al. 2019

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“…In P. aeruginosa , σ SigX has a similar function and absence of this σ factor affects membrane fluidity, fatty acid composition of the cell membrane and cell morphology (Duchesne et al , ; Boechat et al , ; Blanka et al , ; Flechard et al , ). Several conditions that produce cell wall stress increase sigX expression and activity and, in response, σ SigX modulates expression of about 300 genes to relief the stress, including sigX itself (Bouffartigues et al , ; Gicquel et al , ; Blanka et al , ; Bouffartigues et al , ; Chevalier et al , 2019). σ SigX was initially discovered for its function in promoting the transcription of the major outer membrane porin of Pseudomonas , OprF, which is required to maintain cell shape and growth under low osmolarity conditions (Brinkman et al , ).…”

Section: Stress‐responsive Pseudomonas σEcf Factorsmentioning

confidence: 99%

“…cmpX is arranged in an operon with cfrX that is located directly upstream of sigX . Although CfrX does not contain a typical ASD, it contains a short N‐terminal extension present in other genes co‐transcribed with σ ECF genes that may act as σ factor inhibitors and thus CfrX has been proposed as the anti‐σ factor partner of σ SigX (Chevalier et al , ). Regulation of cfrX ‐ cmpX expression by σ SigX has led to the proposal that these three proteins form a new type of mechanosensing transduction system in P. aeruginosa (Chevalier et al , ).…”

Section: Stress‐responsive Pseudomonas σEcf Factorsmentioning

confidence: 99%

“…The GacSA two‐component system is required for hrpL , rpoN and hrpR‐hrpS expression (Chatterjee et al ., ), although how plant signals are perceived and transduced into the Hrp regulatory network remains still poorly understood. Importantly, σ HrpL negatively regulates its own transcription (Waite et al , ), which is not a common feature of Pseudomonas σ ECF factors which usually promote their own expression (Chevalier et al , ). It has been proposed that this negative feedback on σ HrpL activity may fine‐tune T3SS production to minimize the elicitation of plant defenses (Waite et al , ).…”

Section: P Syringae σHrpl Factormentioning

confidence: 99%

“…increased temperature, formation of oxygen‐reactive species or osmotic changes) or by antimicrobial treatments. The P. aeruginosa σ AlgT , σ SigX and σ SbrI factors trigger expression of functions that mitigate stress and maintain the integrity of the bacterial cell envelope (Chevalier et al , ), ensuring the pathogen’s survival. However, these σ factors also promote expression of virulence determinants, like the exopolysaccharide alginate, the elastase LasB, the alkaline metalloproteinase AprA or pro‐inflammatory toxins promoted by σ AlgT (Wood and Ohman, ; Wood and Ohman, ) or the T3SS by σ SigX (Blanka et al , ) .…”

Section: Role Of Pseudomonas σEcf Factors In Virulencementioning

confidence: 99%

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Diversity of extracytoplasmic function sigma (σ^ECF) factor‐dependent signaling in Pseudomonas

Otero-Asman

Wettstadt

Bernal

et al. 2019

Molecular Microbiology

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Pseudomonas bacteria are widespread and are found in soil and water, as well as pathogens of both plants and animals. The ability of Pseudomonas to colonize many different environments is facilitated by the multiple signaling systems these bacteria contain that allow Pseudomonas to adapt to changing circumstances by generating specific responses. Among others, signaling through extracytoplasmic function σ (σ ECF ) factors is extensively present in Pseudomonas. σ ECF factors trigger expression of functions required under particular conditions in response to specific signals. This manuscript reviews the phylogeny and biological roles of σ ECF factors in Pseudomonas, and highlights the diversity of σ ECF -signaling pathways of this genus in terms of function and activation. We show that Pseudomonas σ ECF factors belong to 16 different phylogenetic groups. Most of them are included within the iron starvation group and are mainly involved in iron acquisition. The second most abundant group is formed by RpoE-like σ ECF factors, which regulate the responses to cell envelope stress. Other groups controlling solvent tolerance, biofilm formation and the response to oxidative stress, among other functions, are present in lower frequency. The role of σ ECF factors in the virulence of Pseudomonas pathogenic species is described.

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Cell Envelope Stress Response in Pseudomonas aeruginosa

Chevalier

Bouffartigues

Tortuel

et al. 2022

Advances in Experimental Medicine and Biology

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Extracytoplasmic function sigma factors in Pseudomonas aeruginosa

Cited by 72 publications

References 235 publications

The TonB_m-PocAB System Is Required for Maintenance of Membrane Integrity and Polar Position of Flagella in Pseudomonas putida

The TonB_m-PocAB System Is Required for Maintenance of Membrane Integrity and Polar Position of Flagella in Pseudomonas putida

Diversity of extracytoplasmic function sigma (σ^ECF) factor‐dependent signaling in Pseudomonas

Cell Envelope Stress Response in Pseudomonas aeruginosa

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Extracytoplasmic function sigma factors in Pseudomonas aeruginosa

Cited by 72 publications

References 235 publications

The TonBm-PocAB System Is Required for Maintenance of Membrane Integrity and Polar Position of Flagella in Pseudomonas putida

The TonBm-PocAB System Is Required for Maintenance of Membrane Integrity and Polar Position of Flagella in Pseudomonas putida

Diversity of extracytoplasmic function sigma (σECF) factor‐dependent signaling in Pseudomonas

Cell Envelope Stress Response in Pseudomonas aeruginosa

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Product

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The TonB_m-PocAB System Is Required for Maintenance of Membrane Integrity and Polar Position of Flagella in Pseudomonas putida

The TonB_m-PocAB System Is Required for Maintenance of Membrane Integrity and Polar Position of Flagella in Pseudomonas putida

Diversity of extracytoplasmic function sigma (σ^ECF) factor‐dependent signaling in Pseudomonas