Global Analysis of Extracytoplasmic Stress Signaling in Escherichia coli

Bury‐Moné, Stéphanie; Nomane, Yanoura; Reymond, Nancie; Barbet, Romain; Jacquet, Éric; Imbeaud, Sandrine; Jacq, Annick; Bouloc, Philippe

doi:10.1371/journal.pgen.1000651

Cited by 211 publications

(266 citation statements)

References 97 publications

(172 reference statements)

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“…Although several stress response systems are known to sense and respond to damaged/misfolded membrane proteins (13)(14)(15), there is a paucity of knowledge regarding systems that sense and ameliorate damage to the cell wall. Exceptions are TCS [e.g., WalRK and VraSR (16,17)] found in several Gram-positive genera that respond to exposure to various cell-wall-acting antibiotics by activating regulons that mediate specialized cell wall synthesis/turnover functions.…”

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confidence: 99%

A cell wall damage response mediated by a sensor kinase/response regulator pair enables beta-lactam tolerance

Dörr

Álvarez

Delgado

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The bacterial cell wall is critical for maintenance of cell shape and survival. Following exposure to antibiotics that target enzymes required for cell wall synthesis, bacteria typically lyse. Although several cell envelope stress response systems have been well described, there is little knowledge of systems that modulate cell wall synthesis in response to cell wall damage, particularly in Gram-negative bacteria. Here we describe WigK/WigR, a histidine kinase/response regulator pair that enables Vibrio cholerae, the cholera pathogen, to survive exposure to antibiotics targeting cell wall synthesis in vitro and during infection. Unlike wild-type V. cholerae, mutants lacking wigR fail to recover following exposure to cell-wall–acting antibiotics, and they exhibit a drastically increased cell diameter in the absence of such antibiotics. Conversely, overexpression of wigR leads to cell slimming. Overexpression of activated WigR also results in increased expression of the full set of cell wall synthesis genes and to elevated cell wall content. WigKR-dependent expression of cell wall synthesis genes is induced by various cell-wall–acting antibiotics as well as by overexpression of an endogenous cell wall hydrolase. Thus, WigKR appears to monitor cell wall integrity and to enhance the capacity for increased cell wall production in response to damage. Taken together, these findings implicate WigKR as a regulator of cell wall synthesis that controls cell wall homeostasis in response to antibiotics and likely during normal growth as well.

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confidence: 99%

A cell wall damage response mediated by a sensor kinase/response regulator pair enables beta-lactam tolerance

Dörr

Álvarez

Delgado

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…The maintenance, adaptation, and protection of the bacterial envelope are essential for bacteria. Stresses that damage and alter the bacterial envelope can lead to activation of stress responses in bacteria by means of various phosphorelay signaling systems (5). In E. coli, five different envelope stress responses have been identified: BaeSR, CpxAR, RcsBC, Psp, and E (5,6).…”

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confidence: 99%

“…Stresses that damage and alter the bacterial envelope can lead to activation of stress responses in bacteria by means of various phosphorelay signaling systems (5). In E. coli, five different envelope stress responses have been identified: BaeSR, CpxAR, RcsBC, Psp, and E (5,6). Each response triggers a signaling cascade that leads to the regulation of factors needed to combat envelope damage or to respond to the stress (5).…”

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confidence: 99%

“…In E. coli, five different envelope stress responses have been identified: BaeSR, CpxAR, RcsBC, Psp, and E (5,6). Each response triggers a signaling cascade that leads to the regulation of factors needed to combat envelope damage or to respond to the stress (5). Some envelope stress response signaling has been linked to virulence in Gram-negative bacteria (7,8).…”

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BaeSR, Involved in Envelope Stress Response, Protects against Lysogenic Conversion by Shiga Toxin 2-Encoding Phages

et al. 2015

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Infection and lysogenic conversion with Shiga toxin-encoding bacteriophages (Stx phages) drive the emergence of new Shiga toxin-producing Escherichia coli strains. Phage attachment to the bacterial surface is the first stage of phage infection. Envelope perturbation causes activation of envelope stress responses in bacterial cells. Although many external factors are known to activate envelope stress responses, the role of these responses in the phage-bacterium interaction remains unexplored. Here, we investigate the link between three envelope signaling systems in E. coli (RcsBC, CpxAR, and BaeSR) and Stx2 phage infection by determining the success of bacterial lysogenic conversion. For this purpose, E. coli DH5␣ wild-type (WT) and mutant strains lacking RcsBC, CpxAR, or BaeSR signaling systems were incubated with a recombinant Stx2 phage (933W). Notably, the number of lysogens obtained with the BaeSR mutant was 5 log 10 units higher than with the WT, and the same differences were observed when using 7 different Stx2 phages. To assess whether the membrane receptor used by Stx phages, BamA, was involved in the differences observed, bamA gene expression was monitored by reverse transcription-quantitative PCR (RT-qPCR) in all host strains. A 4-fold-higher bamA expression level was observed in the BaeSR mutant than in the WT strain, suggesting that differential expression of the receptor used by Stx phages accounted for the increase in the number of lysogenization events. Establishing the link between the role of stress responses and phage infection has important implications for understanding the factors affecting lysogenic conversion, which drives the emergence of new pathogenic clones.T emperate phages are responsible for the conversion of nonpathogenic strains of bacteria to pathogenic strains by transduction of virulence genes (1). Well-known examples are Shiga toxin (Stx) phages, which carry the genes for Shiga toxin (stx). Stx phages can cause the conversion of Escherichia coli and bacteria of other genera to Shiga toxin-producing E. coli (STEC) and other Shiga-toxigenic pathogens (2). A recent example is the STEC outbreak in Germany in May 2011, where an enteroaggregative E. coli O104:H4 strain incorporated an Stx2 phage (3, 4). Because the lysogeny of E. coli by Stx phages has relevant implications for their pathogenicity, a better understanding of the molecular mechanisms underlying phage-host interaction is a challenge for researchers and could help in designing strategies to avoid lysogenization by Stx phages.The first step in phage infection is attachment to the specific receptor on the bacterial surface. The maintenance, adaptation, and protection of the bacterial envelope are essential for bacteria. Stresses that damage and alter the bacterial envelope can lead to activation of stress responses in bacteria by means of various phosphorelay signaling systems (5). In E. coli, five different envelope stress responses have been identified: BaeSR, CpxAR, RcsBC, Psp, and E (5, 6). Each response triggers a si...

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“…Its expression is under the control of Bae and Cpx periplasmic stress response systems which are induced by a variety of stress conditions known to cause protein unfolding and aggregation, e.g. heat, urea, ethanol, butanol, all of which use different mechanisms to unfold proteins [4,5]. This suggests that Spy has a general affinity for a wide range of different protein-unfolding intermediates.…”

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confidence: 99%