The alternative sigma factor σE controls antioxidant defences required for Salmonella virulence and stationary‐phase survival

Bacteria must contend with conditions of nutrient limitation in all natural environments. Complex programmes of gene expression, controlled in part by the alternative sigma factors σS (σ38, RpoS) and σH (σ32, RpoH), allow a number of bacterial species to survive conditions of partial or complete starvation. We show here that the alternative sigma factor σE (σ24, RpoE) also facilitates the survival of Salmonella typhimurium under conditions of nutrient deprivation. Expression of the σE regulon is strongly induced upon entry of Salmonella into stationary phase. A Salmonella mutant lacking σE has reduced survival during stationary phase as well as increased susceptibility to oxidative stress. A Salmonella strain lacking both σE and σS is non‐viable after just 24 h in stationary phase, but survival of these mutants is completely preserved under anaerobic stationary‐phase conditions, suggesting that oxidative injury is one of the major mechanisms of reduced microbial viability during periods of nutrient deprivation. Moreover, the attenuated virulence of σE‐deficient Salmonella for mice can be largely restored by genetic abrogation of the host phagocyte respiratory burst, suggesting that the σE regulon plays an important antioxidant role during Salmonella infection of mammalian hosts.

[1]  N. Martin,et al.  Isolation and characterization of a chromosomally encoded disulphide oxidoreductase from Salmonella enterica serovar Typhimurium. , 2001, Canadian journal of microbiology.

[2]  D. Missiakas,et al.  Characterization of the Escherichia coliςE Regulon* , 2001, The Journal of Biological Chemistry.

[3]  D. Missiakas,et al.  Characterization of the Escherichia coli s E Regulon * , 2001 .

[4]  T. Nitta,et al.  Function of the ςE Regulon in Dead-Cell Lysis in Stationary-Phase Escherichia coli , 2000, Journal of bacteriology.

[5]  S. Melov,et al.  Extension of life-span with superoxide dismutase/catalase mimetics. , 2000, Science.

[6]  G. Dougan,et al.  Antimicrobial Actions of the Nadph Phagocyte Oxidase and Inducible Nitric Oxide Synthase in Experimental Salmonellosis. II. Effects on Microbial Proliferation and Host Survival in Vivo , 2000, The Journal of experimental medicine.

[7]  F. Fang,et al.  Antimicrobial Actions of the Nadph Phagocyte Oxidase and Inducible Nitric Oxide Synthase in Experimental Salmonellosis. I. Effects on Microbial Killing by Activated Peritoneal Macrophages in Vitro , 2000, The Journal of experimental medicine.

[8]  V. Deretic,et al.  Dual regulation of mucoidy in Pseudomonas aeruginosa and sigma factor antagonism , 2000, Molecular microbiology.

[9]  N. Fujita,et al.  Two Extracytoplasmic Function Sigma Subunits, ςE and ςFecI, of Escherichia coli: Promoter Selectivity and Intracellular Levels , 2000, Journal of bacteriology.

[10]  Hua,et al.  Identification of , 2000, Journal of insect physiology.

[11]  Sarah E. Ades,et al.  The Escherichia coli sigma(E)-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. , 1999, Genes & development.

[12]  T. Nyström,et al.  Oxidative Stress Defense and Deterioration of Growth-arrestedEscherichia coli Cells* , 1999, The Journal of Biological Chemistry.

[13]  D. Hassett,et al.  Effect of rpoS Mutation on the Stress Response and Expression of Virulence Factors in Pseudomonas aeruginosa , 1999, Journal of bacteriology.

[14]  J. Foster,et al.  Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Valentine,et al.  Mitochondrial superoxide decreases yeast survival in stationary phase. , 1999, Archives of biochemistry and biophysics.

[16]  Manuel Manchado,et al.  In Vivo Transcription of the Escherichia coli oxyRRegulon as a Function of Growth Phase and in Response to Oxidative Stress , 1999, Journal of bacteriology.

[17]  M. Roberts,et al.  The Alternative Sigma Factor, ςE, Is Critically Important for the Virulence of Salmonella typhimurium , 1999, Infection and Immunity.

[18]  M. Roberts,et al.  The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. , 1999, Infection and immunity.

[19]  R. Kolter,et al.  Role of the Escherichia coli SurA Protein in Stationary-Phase Survival , 1998, Journal of bacteriology.

[20]  T. Nyström,et al.  Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon. , 1998, Genes & development.

[21]  D. Missiakas,et al.  The extracytoplasmic function sigma factors: role and regulation , 1998, Molecular microbiology.

[22]  S. Cadenas,et al.  The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach , 1998, Journal of Comparative Physiology B.

[23]  M. Spector The starvation-stress response (SSR) of Salmonella. , 1998, Advances in microbial physiology.

[24]  F. Fang,et al.  Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Hsieh,et al.  Growth-phase-dependent transcriptional regulation of the pcm and surE genes required for stationary-phase survival of Escherichia coli. , 1997, Microbiology.

[26]  C. Gross,et al.  SigmaE is an essential sigma factor in Escherichia coli , 1997, Journal of bacteriology.

[27]  F. Fang,et al.  SlyA, a transcriptional regulator of Salmonella typhimurium, is required for resistance to oxidative stress and is expressed in the intracellular environment of macrophages , 1997, Infection and immunity.

[28]  T. Silhavy,et al.  The sigma(E) and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. , 1997, Genes & development.

[29]  R. Husson,et al.  A mycobacterial extracytoplasmic function sigma factor involved in survival following stress , 1997, Journal of bacteriology.

[30]  C. Georgopoulos,et al.  Modulation of the Escherichia coliσE (RpoE) heat‐shock transcription‐factor activity by the RseA, RseB and RseC proteins , 1997, Molecular microbiology.

[31]  C. Gross,et al.  The σE‐mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of σE , 1997, Molecular microbiology.

[32]  D. Touati,et al.  Hypochlorous acid stress in Escherichia coli: resistance, DNA damage, and comparison with hydrogen peroxide stress , 1996, Journal of bacteriology.

[33]  J. Betton,et al.  New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH , 1996, Molecular microbiology.

[34]  N. Hibler,et al.  Virulence properties of Pseudomonas aeruginosa lacking the extreme-stress sigma factor AlgU (sigmaE) , 1996, Infection and immunity.

[35]  A. Kornberg,et al.  Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli , 1996, Journal of bacteriology.

[36]  S. Mongkolsuk,et al.  Regulation of the oxidative stress protective enzymes, catalase and superoxide dismutase in Xanthomonas--a review. , 1996, Gene.

[37]  M. Levinthal,et al.  hns, rpoS and lrp mutations affect stationary-phase survival at high osmolarity. , 1996, Research in microbiology.

[38]  D. Looney,et al.  HIV gp120-specific cell-mediated immune responses in mice after oral immunization with recombinant Salmonella. , 1995, Journal of acquired immune deficiency syndromes and human retrovirology : official publication of the International Retrovirology Association.

[39]  F. Heffron,et al.  Fur regulon of Salmonella typhimurium: identification of new iron-regulated genes , 1995, Journal of bacteriology.

[40]  C. Nathan,et al.  Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase , 1995, Cell.

[41]  K. Makino,et al.  The rpoE gene of Escherichia coli, which encodes sigma E, is essential for bacterial growth at high temperature , 1995, Journal of bacteriology.

[42]  C. Georgopoulos,et al.  The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli. , 1995, The EMBO journal.

[43]  K. Rudd,et al.  rpoE, the gene encoding the second heat‐shock sigma factor, sigma E, in Escherichia coli. , 1995, The EMBO journal.

[44]  N. Brot,et al.  Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage , 1995, Journal of bacteriology.

[45]  H. Shinagawa,et al.  TherpoEGene ofEscherichia coli, Which Encodes s E , Is Essential for Bacterial Growth at High Temperature , 1995 .

[46]  J. Foster,et al.  How Salmonella survive against the odds. , 1995, Annual review of microbiology.

[47]  David A. Williams,et al.  Mouse model of X–linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production , 1995, Nature Genetics.

[48]  D. Martin,et al.  Analysis of promoters controlled by the putative sigma factor AlgU regulating conversion to mucoidy in Pseudomonas aeruginosa: relationship to sigma E and stress response , 1994, Journal of bacteriology.

[49]  K. Rudd,et al.  Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[50]  T. Mizuno,et al.  An analogue of the DnaJ molecular chaperone whose expression is controlled by σS during the stationary phase and phosphate starvation in Escherichia coli , 1994, Molecular microbiology.

[51]  F. Fang,et al.  RpoS is necessary for both the positive and negative regulation of starvation survival genes during phosphate, carbon, and nitrogen starvation in Salmonella typhimurium , 1994, Journal of bacteriology.

[52]  R. Hengge-aronis,et al.  The role of the sigma factor sigma S (KatF) in bacterial global regulation. , 1994, Annual review of microbiology.

[53]  T. Donohue,et al.  The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. , 1993, Genes & development.

[54]  F. Heffron,et al.  Recombination‐deficient mutants of Salmonella typhimurium are avirulent and sensitive to the oxidative burst of macrophages , 1993, Molecular microbiology.

[55]  R. Kolter,et al.  The stationary phase of the bacterial life cycle. , 1993, Annual review of microbiology.

[56]  F. Fang,et al.  The alternative sigma factor katF (rpoS) regulates Salmonella virulence. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[57]  C. Miller,et al.  Escherichia coli genes involved in cell survival during dormancy: role of oxidative stress. , 1992, Biochemical and biophysical research communications.

[58]  G. Cornelis,et al.  A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. , 1991, Gene.

[59]  A. Matin,et al.  The putative sigma factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli , 1991, Journal of bacteriology.

[60]  R. Kolter,et al.  Stationary-phase-inducible "gearbox" promoters: differential effects of katF mutations and role of sigma 70 , 1991, Journal of bacteriology.

[61]  I. Blomfield,et al.  Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature‐sensitive pSC101 replicon , 1991, Molecular microbiology.

[62]  A. Matin,et al.  Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival , 1991, Journal of bacteriology.

[63]  I. Charles,et al.  The role of a stress‐response protein in Salmonella typhimurium virulence , 1991, Molecular microbiology.

[64]  R. Hengge-aronis,et al.  Identification of a central regulator of stationary‐phase gene expression in Escherichia coli , 1991, Molecular microbiology.

[65]  C. Gross,et al.  Identification of the sigma E subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression. , 1989, Genes & development.

[66]  J. Kaguni,et al.  A novel sigma factor is involved in expression of the rpoH gene of Escherichia coli , 1989, Journal of bacteriology.

[67]  D. Touati,et al.  Exonuclease III and the catalase hydroperoxidase II in Escherichia coli are both regulated by the katF gene product. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[68]  W. Bullock XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. , 1987 .

[69]  R. Simons,et al.  Improved single and multicopy lac-based cloning vectors for protein and operon fusions. , 1987, Gene.

[70]  S. Linn,et al.  Bimodal pattern of killing of DNA-repair-defective or anoxically grown Escherichia coli by hydrogen peroxide , 1986, Journal of bacteriology.

[71]  B. Bochner Curing bacterial cells of lysogenic viruses by using ucb indicator plates , 1984 .

[72]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[73]  D. Hanahan Studies on transformation of Escherichia coli with plasmids. , 1983, Journal of molecular biology.

[74]  P. Loewen Levels of glutathione in Escherichia coli. , 1979, Canadian journal of biochemistry.

[75]  A. C. Chang,et al.  Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid , 1978, Journal of bacteriology.

[76]  Jeffrey H. Miller Experiments in molecular genetics , 1972 .