The starvation-stress response of Salmonella enterica serovar Typhimurium requires σE-, but not CpxR-regulated extracytoplasmic functions

Kenyon, William J.; Sayers, D. Geary; Humphreys, Sue; Roberts, Mark; Spector, Michael P.

doi:10.1099/00221287-148-1-113

Cited by 51 publications

(70 citation statements)

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“…In the saline starvation-survival model used, nutrient starvation (Spector, 1998;Kenyon et al, 2002) and oxidative stress (Humphreys et al, 1999;Testerman et al, 2002;Kenyon et al, 2002) are likely to contribute to cell envelope stress and ultimately to death of the cell. The death rate of a bacterial population that has defects in regulation of metabolic activity under starvation conditions is thus likely to be more rapid.…”

Section: Resultsmentioning

confidence: 99%

“…S. Typhimurium SL1344 wild-type (WT) (Hoiseth & Stocker, 1981) and mutant strains were stored at 280 uC on cryobeads (Prolab diagnostics). S. Typhimurium strains with null mutations in rpoE (Humphreys et al, 1999) or rpoS, and a double mutant (rpoE/rpoS) (Kenyon et al, 2002) were used. Prior to each experiment, the appropriate strain was recovered by spreading a bead onto Colombia agar containing 5 % defibrinated horse blood (BA; Oxoid) and incubated overnight at 37 uC.…”

Section: Methodsmentioning

confidence: 99%

“…Starvation for certain nutrients renders S. Typhimurium more resilient than nutrient-replete cells to a variety of stresses (the starvation stress response) and this is also mediated by both s E and s S (Spector & Cubitt, 1992;Kenyon et al, 2002). Both sigma factors also participate in the pathogenesis of S. Typhimurium infection (Fang et al, 1992;Nickerson & Curtiss, 1997;Humphreys et al, 1999;Testerman et al, 2002;Rowley et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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Role of the alternative sigma factors σ E and σ S in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock

et al. 2007

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The ability of Salmonella enterica serovar Typhimurium to survive environmental stress requires specific, coordinated, responses, which induce resistance to the stress condition. This study investigated the relative contribution of s E and s S , the sigma factors regulating extracytoplasmic and general stress response functions, respectively, to survival at low temperature and also in media of differing osmotic strength, conditions relevant to food preservation. To determine if low-temperature storage is a signal for s E -and s S -mediated survival, the ability of S. Typhimurium rpoE, rpoS and rpoE/rpoS mutants to survive in a saline starvation-survival model at a refrigeration temperature (4.5 6C) was examined. Under these conditions, the rpoE mutant was significantly (P<0.05) compromised compared to the parent and to an rpoS mutant. The double mutant in rpoE and rpoS displayed a cumulative defect in survival. In hyperosmotic environments (low a w ) containing 6 % NaCl and at refrigeration temperature, both sigma factors were important for maximum survival but s S played the dominant role. Analysis of the metabolic activity of starved populations at 4.5 and 37 6C revealed significantly (P<0.001) elevated electron-transport system activity in mutants in rpoE and rpoS, indicating a role for s E -and s S -regulated genes in maintaining energy homeostasis. Together these data demonstrate that s E and s S are important for survival of S. Typhimurium in conditions encountered during food processing and that the relative contribution of s E and s S is critically dependent on the precise nature of the stress.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Role of the alternative sigma factors σ E and σ S in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock

et al. 2007

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“…Inactivation of E in E. coli is lethal, and existing rpoE mutants contain suppressive mutations (10,16). In other bacteria, like Salmonella enterica serovar Typhimurium, the resistance to multiple stresses, as well as the survival in stationary phase, of rpoE mutants is affected (32,37,66).…”

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An Extracytoplasmic Function Sigma Factor Acts as a General Stress Response Regulator inSinorhizobium meliloti

et al. 2007

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Sinorhizobium meliloti genes transcriptionally up-regulated after heat stress, as well as upon entry into stationary phase, were identified by microarray analyses. Sixty stress response genes were thus found to be up-regulated under both conditions. One of them, rpoE2 (smc01506), encodes a putative extracytoplasmic function (ECF) sigma factor. We showed that this sigma factor controls its own transcription and is activated by various stress conditions, including heat and salt, as well as entry into stationary phase after either carbon or nitrogen starvation. We also present evidence that the product of the gene cotranscribed with rpoE2 negatively regulates RpoE2 activity, and we therefore propose that it plays the function of anti-sigma factor. By combining transcriptomic, bioinformatic, and quantitative reverse transcription-PCR analyses, we identified 44 RpoE2-controlled genes and predicted the number of RpoE2 targets to be higher. Strikingly, more than one-third of the 60 stress response genes identified in this study are RpoE2 targets. Interestingly, two genes encoding proteins with known functions in stress responses, namely, katC and rpoH2, as well as a second ECF-encoding gene, rpoE5, were found to be RpoE2 regulated. Altogether, these data suggest that RpoE2 is a major global regulator of the general stress response in S. meliloti. Despite these observations, and although this sigma factor is well conserved among alphaproteobacteria, no in vitro nor in planta phenotypic difference from the wild-type strain could be detected for rpoE2 mutants. This therefore suggests that other important actors in the general stress response have still to be identified in S. meliloti.To survive the many stress conditions that they encounter in nature, bacteria have evolved rapid responses that result in the prevention or repair of cellular damages caused by stresses. In addition to these usually stress-specific responses, more general stress responses take place in reaction to a variety of insults as different as high osmolarity, heat or cold shock, pH variation, and nutrient starvation (which results in stationary phase). One well-known consequence of these general stress responses is the ability of bacteria to resist stress better in stationary phase than in exponential phase. This phenomenon, observed in most bacterial species studied so far, is considered a universal way for these microorganisms to survive not only the stress that they currently experience, but also stress conditions that they could potentially face in the future, and is therefore of primary importance in nature, where bacteria often are nutrient or oxygen limited and where environmental conditions constantly change (28).Much of our knowledge regarding the mechanisms of induction of general stress responses derives from studies of the model bacterium Escherichia coli and its close relatives. In these bacteria, entry into stationary phase, as well as a number of different stress conditions, leads to the activation of alternative sigma factors, which re...

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“…Alternative factors have been shown in various bacteria to be of importance for survival under extreme conditions (7,14,23,31,38,44,49,60,68,73,78,79,80) and to influence virulence and pathogenicity (8,13,32,35,37,42,51,57,61,71,75,78,81).…”

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Microarray-Based Analysis of theStaphylococcus aureusσ^BRegulon

et al. 2004

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Microarray-based analysis of the transcriptional profiles of the genetically distinct Staphylococcus aureus strains COL, GP268, and Newman indicate that a total of 251 open reading frames (ORFs) are influenced by B activity. While B was found to positively control 198 genes by a factor of >2 in at least two of the three genetic lineages analyzed, 53 ORFs were repressed in the presence of B . Gene products that were found to be influenced by B are putatively involved in all manner of cellular processes, including cell envelope biosynthesis and turnover, intermediary metabolism, and signaling pathways. Most of the genes and/or operons identified as upregulated by B were preceded by a nucleotide sequence that resembled the B consensus promoter sequence of Bacillus subtilis. A conspicuous number of virulence-associated genes were identified as regulated by B activity, with many adhesins upregulated and prominently represented in this group, while transcription of various exoproteins and toxins were repressed. The data presented here suggest that the B of S. aureus controls a large regulon and is an important modulator of virulence gene expression that is likely to act conversely to RNAIII, the effector molecule of the agr locus. We propose that this alternative transcription factor may be of importance for the invading pathogen to fine-tune its virulence factor production in response to changing host environments.Transcription of DNA into RNA is catalyzed by RNA polymerase. In bacteria, one RNA polymerase generates nearly all cellular RNAs, including ribosomal, transfer, and mRNA. This enzyme consists of six subunits, ␣ 2 ␤␤Ј, with ␣ 2 ␤␤Ј forming the catalytically competent RNA polymerase core enzyme (E). The core is capable of elongation and termination of transcription, but it is unable to initiate transcription at specific promoter sequences. The subunit, which when bound to E forms the holoenzyme (E-), directs the multisubunit complex to specific promoter elements and allows efficient initiation of transcription (reviewed in references 5 and 6). Therefore, factors provide an elegant mechanism in eubacteria to allow simultaneous transcription of a variety of genetically unlinked genes, provided all of these genes share the same promoter specificities.In addition to the housekeeping sigma subunit, 70 or A , most bacteria produce one or more additional subunits, termed alternative factors, which direct the respective Ecomplex to distinct classes of promoters that contain alternative factor-specific sequences. Alternative factors have been shown in various bacteria to be of importance for survival under extreme conditions (7,14,23,31,38,44,49,60,68,73,78,79,80) and to influence virulence and pathogenicity (8,13,32,35,37,42,51,57,61,71,75,78,81).At least six alternative factors are produced by the enteric bacterium Escherichia coli (reviewed in reference 6). Genomic sequence analysis suggests that many alternative factors also exist in a number of other pathogenic species such as Treponema palladium (4 alternative f...

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The starvation-stress response of Salmonella enterica serovar Typhimurium requires σE-, but not CpxR-regulated extracytoplasmic functions

Cited by 51 publications

References 48 publications

Role of the alternative sigma factors σ E and σ S in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock

Role of the alternative sigma factors σ E and σ S in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock

An Extracytoplasmic Function Sigma Factor Acts as a General Stress Response Regulator inSinorhizobium meliloti

Microarray-Based Analysis of theStaphylococcus aureusσ^BRegulon

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The starvation-stress response of Salmonella enterica serovar Typhimurium requires σE-, but not CpxR-regulated extracytoplasmic functions

Cited by 51 publications

References 48 publications

Role of the alternative sigma factors σ E and σ S in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock

Role of the alternative sigma factors σ E and σ S in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock

An Extracytoplasmic Function Sigma Factor Acts as a General Stress Response Regulator inSinorhizobium meliloti

Microarray-Based Analysis of theStaphylococcus aureusσBRegulon

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Product

Resources

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Microarray-Based Analysis of theStaphylococcus aureusσ^BRegulon