Archives of Microbiology

, Volume 181, Issue 4, pp 255–268 | Cite as

Incidence and function of sigma factors in Ralstonia metallidurans and other bacteria



Bacterial sigma factors are essential for directing the bacterial RNA polymerase to promoter regions during transcription initiation. Genomic sequencing of the highly heavy-metal-resistant β-proteobacterium Ralstonia metallidurans strain CH34 revealed 17 candidate genes for sigma factors. This review compares the sigma factor machinery of R. metallidurans to that of other bacteria. The sigma factors of 105 bacterial genomes were assigned to sigma factor clusters and families formed around the factors from Escherichia coli, Bacillus subtilis, and R. metallidurans. Genes for between 1 and 65 sigma-factor-related proteins were found in these genomes. Although prediction of sigma factor function from sequence comparisons can be misleading, organization of the R. metallidurans sigma factors into clusters and protein families, together with a discussion of the physiological function of members of these clusters, might yield insight into the cellular roles of bacterial sigma factors and the genes that depend on them for their expression.


Sigma factors Extracytoplasmic function Alcaligenes eutrophus Ralstonia metallidurans 

Supplementary material

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Supplementary material (PDF 163 KB)


  1. Ades SE, Grigorova IL, Gross CA (2003) Regulation of the alternative sigma factor σE during initiation, adaptation, and shutoff of the extracytoplasmic heat shock response in Escherichia coli. J Bacteriol 185:2512–2519CrossRefPubMedGoogle Scholar
  2. Aguilar C, Bertani I, Venturi V (2003) Quorum-sensing system and stationary-phase sigma factor (rpoS) of the onion pathogen Burkholderia cepacia genomovar I type strain, ATCC 25416. Appl Environ Microbiol 69:1739–1747CrossRefPubMedGoogle Scholar
  3. Arcuri EF, Wiedmann M, Boor KJ (2000) Phylogeny and functional conservation of σE in endospore-forming bacteria. Microbiology (UK) 146:1593–1603Google Scholar
  4. Asai K, Yamaguchi H, Kang CM, Yoshida K, Fujita Y, Sadaie Y (2003) DNA microarray analysis of Bacillus subtilis sigma factors of extracytoplasmic function family. FEMS Microbiol Lett 220:155–160CrossRefPubMedGoogle Scholar
  5. Barne KA, Bown JA, Busby SJ, Minchin SD (1997) Region 2.5 of the Escherichia coli RNA polymerase sigma70 subunit is responsible for the recognition of the ‘extended-10’ motif at promoters. EMBO J 16:4034–4040CrossRefPubMedGoogle Scholar
  6. Barrios H, Valderrama B, Morett E (1999) Compilation and analysis of sigma 54-dependent promoter sequences. Nucleic Acids Res 27:4305–4313PubMedGoogle Scholar
  7. Bordes P, Conter A, Morales V, Bouvier J, Kolb A, Gutierrez C (2003) DNA supercoiling contributes to disconnect σS accumulation from σS-dependent transcription in Escherichia coli. Mol Microbiol 48:561–571CrossRefPubMedGoogle Scholar
  8. Braun V, Mahren S, Ogierman M (2003) Regulation of the Fecl-type ECF sigma factor by transmembrane signalling. Curr Opin Microbiol 6:173–180CrossRefPubMedGoogle Scholar
  9. Brigulla M, Hoffmann T, Krisp A, Volker A, Bremer E, Völker U (2003) Chill induction of the SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation. J Bacteriol 185:4305–4314CrossRefPubMedGoogle Scholar
  10. Brinkman FSL, Schoofs G, Hancock REW, De Mot R (1999) Influence of a putative ECF sigma factor on expression of the major outer membrane protein, OprF, in Pseudomonas aeruginosa and Pseudomonas fluorescens. J Bacteriol 181:4746–4754PubMedGoogle Scholar
  11. Britton RA, Eichenberger P, Gonzalez-Pastor JE, Fawcett P, Monson R, Losick R, Grossman AD (2002) Genome-wide analysis of the stationary-phase sigma factor σH regulon of Bacillus subtilis. J Bacteriol 184:4881–4890CrossRefPubMedGoogle Scholar
  12. Brown L, Gentry D, Elliott T, Cashel M (2002) DksA affects ppGpp induction of RpoS at a translational level. J Bacteriol 184:4455–4465CrossRefPubMedGoogle Scholar
  13. Burger M, Woods RG, McCarthy C, Beacham R (2000) Temperature regulation of protease in Pseudomonas fluorescens LS107d2 by an ECF sigma factor and a transmembrane activator. Microbiology (UK) 146:3149–3155Google Scholar
  14. Camarero JA, Shekhtman A, Campbell EA, Chlenov M, Gruber TM, Bryant DA, Darst SA, Cowburn D, Muir TW (2002) Autoregulation of a bacterial sigma factor explored by using segmental isotopic labeling and NMR. Proc Natl Acad Sci USA 99:8536–8541CrossRefPubMedGoogle Scholar
  15. Cao M, Helmann JD (2002) Regulation of the Bacillus subtilis bcrC bacitracin resistance gene by two extracytoplasmic function sigma factors. J Bacteriol 184:6123–6129CrossRefPubMedGoogle Scholar
  16. Cao M, Kobel PA, Morshedi MM, Wu MFW, Paddon C, Helmann JD (2002) Defining the Bacillus subtilis σW regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. J Mol Biol 316:443–457CrossRefPubMedGoogle Scholar
  17. Cao M, Salzberg L, Tsai CS, Mascher T, Bonilla C, Wang T, Ye RW, Marquez-Magana L, Helmann JD (2003) Regulation of the Bacillus subtilis extracytoplasmic function protein σY and its target promoters. J Bacteriol 185:4883–4890CrossRefPubMedGoogle Scholar
  18. Carlson HC, Lu S, Kroos L, Haldenwang WG (1996) Exchange of precursor-specific elements between Pro-sigma E and Pro-sigma K of Bacillus subtilis. J Bacteriol 178:546–549PubMedGoogle Scholar
  19. Cashel M, Hsu LM, Hernandez VJ (2003) Changes in conserved region 3 of Escherichia coli σ70 reduce abortive transcription and enhance promoter escape. J Biol Chem 278:5539–5547CrossRefPubMedGoogle Scholar
  20. Chen C-C, Lewis RJ, Harris R, Yudkin MD, Delumeau O (2003) A supramolecular complex in the environmental stress signalling pathway of Bacillus subtilis. Mol Microbiol 49:1657–1669CrossRefPubMedGoogle Scholar
  21. Child M, Strike P, Pickup R, Edwards C (2002) Salmonella typhimurium displays cyclical patterns of sensitivity to UV-C killing during prolonged incubation in the stationary phase of growth. FEMS Microbiol Lett 213:81–85CrossRefPubMedGoogle Scholar
  22. Collinet B, Yuzawa H, Chen T, Herrera C, Missiakas D (2000) RseB binding to the periplasmic domain of RseA modulates the RseA:σE interaction in the cytoplasm and the availability of σE RNA polymerase. J Biol Chem 275:33898–33904CrossRefPubMedGoogle Scholar
  23. Dartigalongue C, Missiakas D, Raina S (2001) Characterization of the Escherichia coli σE regulon. J Biol Chem 276:20866–20875CrossRefPubMedGoogle Scholar
  24. Deretic DWRaV (2000) Membrane-to-cytosol redistribution of ECF sigma factor AlgU and conversion to mucoidy in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Mol Microbiol 36:314–327CrossRefPubMedGoogle Scholar
  25. Dove SL, Darst SA, Hochschild A (2003) Region 4 of sigma as a target for transcription regulation. Mol Microbiol 48:863–874CrossRefPubMedGoogle Scholar
  26. Enz S, Brand H, Orellana C, Mahren S, Braun V (2003a) Sites of interaction between the FecA and FecR signal transduction proteins of ferric citrate transport in Escherichia coli K-12. J Bacteriol 185:3745–3752CrossRefPubMedGoogle Scholar
  27. Enz S, Mahren S, Menzel C, Braun V (2003b) Analysis of the ferric citrate transport gene promoter of Escherichia coli. J Bacteriol 185:2387–2391CrossRefPubMedGoogle Scholar
  28. Errington J (2003) Regulation of endospore formation in Bacillus subtilis. Nat Rev Microbiol 1:117–126CrossRefGoogle Scholar
  29. Errington J, Feucht A, Lewis PJ, Lord M, Magnin T, Najafi SM, Wilkinson JF, Yudkin MD (1996) Control of the cell-specificity of σF activity in Bacillus subtilis. Phil Trans R Soc Lond B Biol Sci 351:537–542Google Scholar
  30. Fernandes ND, Wu QL, Kong DQ, Puyang XL, Garg S, Husson RN (1999) A mycobacterial extracytoplasmic sigma factor involved in survival following heat shock and oxidative stress. J Bacteriol 181:4266–4274PubMedGoogle Scholar
  31. Feucht A, Evans L, Errington J (2003) Identification of sporulation genes by genome-wide analysis of the σE regulon of Bacillus subtilis. Microbiology (UK) 149:3023–3034Google Scholar
  32. Firoved AM, Boucher JC, Deretic V (2002) Global genomic analysis of AlgU (σE)-dependent promoters (sigmulon) in Pseudomonas aeruginosa and implications for inflammatory processes in cystic fibrosis. J Bacteriol 184:1057–1064CrossRefPubMedGoogle Scholar
  33. Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR, Cartinhour S, Chatterjee AK, D’Ascenzo M, Gwinn ML, Lazarowitz SG, Lin N-C, Martin GB, Rehm AH, Schneider DJ, van Dijk K, Tang X, Collmer A (2002) Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc Natl Acad Sci USA 99:2275–2280CrossRefPubMedGoogle Scholar
  34. Franke S, Grass G, Rensing C, Nies DH (2003) Molecular analysis of the copper-transporting CusCFBA efflux system from Escherichia coli. J Bacteriol 185:3804–3812CrossRefPubMedGoogle Scholar
  35. Fujita M (2000) Temporal and selective association of multiple sigma factors with RNA polymerase during sporulation in Bacillus subtilis. Genes Cells 5:79–88CrossRefPubMedGoogle Scholar
  36. Gamer J, Multhaup G, Tomoyasu T, McCarty JS, Rudiger S, Schönfeld H, Schirra C, Bujard H, Bukau B (1996) A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates activity of the Escherichia coli heat shock transcription factor σ32. EMBO J 15:607–615PubMedGoogle Scholar
  37. Gardella T, Moyle H, Susskind MM (1989) A mutant Escherichia coli sigma 70 subunit of RNA polymerase with altered promoter specificity. J Mol Biol 206:579–590PubMedGoogle Scholar
  38. Gowrishankar J, Yamamoto K, Subbarayan PR, Ishihama A (2003) In vitro properties of RpoS (σS) mutants of Escherichia coli with postulated N-terminal subregion 1.1 or C-terminal region 4 deleted. J Bacteriol 185:2673–2679CrossRefPubMedGoogle Scholar
  39. Grass G, Große C, Nies DH (2000) Regulation of the cnr cobalt/nickel resistance determinant from Ralstonia sp. CH34. J Bacteriol 182:1390–1398CrossRefPubMedGoogle Scholar
  40. Gross CA, Chan C, Dombroski A, Gruber T, Sharp M, Tupy J, Young B (1998) The functional and regulatory roles of sigma factors in transcription. Cold Spring Harb Symp Quant Biol 63:141–155PubMedGoogle Scholar
  41. Große C, Grass G, Anton A, Franke S, Navarrete Santos A, Lawley B, Brown NL, Nies DH (1999) Transcriptional organization of the czc heavy metal homoeostasis determinant from Alcaligenes eutrophus. J Bacteriol 181:2385–2393PubMedGoogle Scholar
  42. Gruber TM, Bryant DA (1997) Molecular systematic studies of eubacteria, using sigma70-type sigma factors of group 1 and group 2. J Bacteriol 179:1734–1747PubMedGoogle Scholar
  43. Haldenwang WG (1995) The sigma factors of Bacillus subtilis. Microbiol Rev 59:1–30PubMedGoogle Scholar
  44. Harley CB, Reynolds RP (1987) Analysis of E. coli promoter sequences. Nucleic Acids Res 15:2343–2361PubMedGoogle Scholar
  45. Hecker M, Schumann W, Völker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19:417–428PubMedGoogle Scholar
  46. Helmann JD (2002) The extracytoplasmic (ECF) sigma factors. Adv Microbiol Physiol 46:47–110Google Scholar
  47. Hengge-Aronis R (2002) Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66:373–395CrossRefPubMedGoogle Scholar
  48. Heungens K, Cowles CE, Goodrich-Blair H (2002) Identification of Xenorhabdus nematophila genes required for mutualistic colonization of Steinernema carpocapsae nematodes. Mol Microbiol 45:1337–1353CrossRefPubMedGoogle Scholar
  49. Hirsch M, Elliott T (2002) Role of ppGpp in rpoS stationary-phase regulation in Escherichia coli. J Bacteriol 184:5077–5087CrossRefPubMedGoogle Scholar
  50. Horsburgh MJ, Moir A (1999) σM, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt. Mol Microbiol 32:41–50CrossRefPubMedGoogle Scholar
  51. Horsburgh MJ, Thackray PD, Moir A (2001) Transcriptional responses during outgrowth of Bacillus subtilis endospores. Microbiology (UK) 147:2933–2941Google Scholar
  52. Huang XJ, Fredrick KL, Helmann JD (1998) Promoter recognition by Bacillus subtilis σW: autoregulation and partial overlap with the σX regulon. J Bacteriol 180:3765–3770PubMedGoogle Scholar
  53. Huang XJ, Gaballa A, Cao M, Helmann JD (1999) Identification of target promoters for the Bacillus subtilis extracytoplasmic function sigma factor, σW. Mol Microbiol 31:361–371CrossRefPubMedGoogle Scholar
  54. Hughes KT, Mathee K (1998) The anti-sigma factors. Annu Rev Microbiol 52:231–286PubMedGoogle Scholar
  55. Imamura S, Yoshihara S, Nakano S, Shiozaki N, Yamada A, Tanaka K, Takahashi H, Asayama M, Shirai M (2003) Purification, characterization, and gene expression of all sigma factors of RNA polymerase in a cyanobacterium. J Mol Biol 325:857–872CrossRefPubMedGoogle Scholar
  56. Jarmer H, Larsen TS, Krogh A, Saxild HH, Brunak S, Knudsen S (2001) Sigma A recognition sites in the Bacillus subtilis genome. Microbiology (UK) 147:2417–2424Google Scholar
  57. Jishage M, Ishihama A (1995) Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of sigma 70 and sigma 38. J Bacteriol 177:6832–6835PubMedGoogle Scholar
  58. Jishage M, Ishihama A (1998) A stationary phase protein in Escherichia coli with binding activity to the major [sigma] subunit of RNA polymerase. Proc Natl Acad Sci USA 95:4953–4958CrossRefPubMedGoogle Scholar
  59. Jishage M, Dasgupta D, Ishihama A (2001) Mapping of the contact site on the sigma 70 subunit of Escherichia coli RNA polymerase. J Bacteriol 183:2952–2956CrossRefPubMedGoogle Scholar
  60. Ju J, Haldenwang WG (2003) Tethering of the Bacillus subtilis σE proprotein to the cell membrane is necessary for its processing but insufficient for its stabilization. J Bacteriol 185:5897–5900CrossRefPubMedGoogle Scholar
  61. Ju J, Mitchell T, Peters Hr, Haldenwang WG (1999) Sigma factor displacement from RNA polymerase during Bacillus subtilis sporulation. J Bacteriol 181:4969–4977PubMedGoogle Scholar
  62. Juhnke S, Peitzsch N, Hübener N, Große C, Nies DH (2002) New genes involved in chromate resistance in Ralstonia metallidurans strain CH34. Arch Microbiol 179:15–25CrossRefPubMedGoogle Scholar
  63. Jung IL, Kim IG (2003) Transcription of ahpC, katG, and katE genes in Escherichia coli is regulated by polyamines: polyamine-deficient mutant sensitive to H2O2-induced oxidative damage. Biochem Biophys Res Commun 301:915–922CrossRefPubMedGoogle Scholar
  64. Kanehara K, Ito K, Akiyama Y (2002) YaeL (EcfE) activates the σE pathway of stress response through a site-2 cleavage of anti-σE, RseA. Genes Dev 16:2147–2155CrossRefPubMedGoogle Scholar
  65. Karls RK, Brooks J, Rossmeissl P, Luedke J, Donohue TJ (1998) Metabolic roles of a Rhodobacter sphaeroides member of the sigma 32 family. J Bacteriol 180:10–19PubMedGoogle Scholar
  66. Kenyon WJ, Sayers DG, Humphreys S, Roberts M, Spector MP (2002) The starvation-stress response of Salmonella enterica serovar Typhimurium requires σE-, but not CpxR-regulated extracytoplasmic functions. Microbiology (UK) 148:113–122Google Scholar
  67. King N, Dreesen O, Stragier P, Pogliano K, Losick R (1999) Septation, dephosphorylation, and the activation of sigmaF during sporulation in Bacillus subtilis. Genes Dev 13:1156–1167PubMedGoogle Scholar
  68. Klein G, Dartigalongue C, Raina S (2003) Phosphorylation-mediated regulation of heat shock response in Escherichia coli. Mol Microbiol 48:269–285PubMedGoogle Scholar
  69. Kutsukake K (1994) Excretion of the anti-sigma factor through a flagellar substructure couples flagellar assembly in Salmonella typhimurium. Mol Gen Genet 243:605–612PubMedGoogle Scholar
  70. Kutsukake K, Iino T (1994) Role of the FliA-FlgM regulatory system in the transcriptional control of the flagellar formation in Salmonella typhimurium. J Bacteriol 176:3598–3605PubMedGoogle Scholar
  71. Lacour S, Kolb A, Landini P (2003) Nucleotides from −16 to −12 determine specific promoter recognition by bacterial σS-RNA polymerase. J Biol Chem 278:37160–37168CrossRefPubMedGoogle Scholar
  72. Layton JC, Foster PL (2003) Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli. Mol Microbiol 502:549–561CrossRefGoogle Scholar
  73. Lee SJ, Gralla JD (2002) Promoter use by σ38 (RpoS) RNA polymerase—amino acid clusters for DNA binding and isomerization. J Biol Chem 277:47420–47427CrossRefPubMedGoogle Scholar
  74. Lee SJ, Gralla JD (2003) Open complex formation in vitro by σ38 (RpoS) RNA polymerase: roles for region 2 amino acids. J Mol Biol 329:941–948CrossRefPubMedGoogle Scholar
  75. Legatzki A, Anton A, Grass G, Rensing C, Nies DH (2003a) Interplay of the Czc-system and two P-type ATPases in conferring metal resistance to Ralstonia metallidurans. J Bacteriol 185:4354–4361CrossRefPubMedGoogle Scholar
  76. Legatzki A, Franke S, Lucke S, Hoffmann T, Anton A, Neumann D, Nies DH (2003b) First step towards a quantitative model describing Czc-mediated heavy metal resistance in Ralstonia metallidurans. Biodegradation 14:153–168CrossRefPubMedGoogle Scholar
  77. Lehnen D, Blumer C, Polen T, Wackwitz B, Wendisch VF, Unden G (2002) LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol Microbiol 45:521–532CrossRefPubMedGoogle Scholar
  78. Libereck K, Wall D, Georgopoulos C (1995) The DnaJ chaperone catalytically activates the DnaK chaperone to preferentially bind σ32 heat shock transcriptional regulator. Proc Natl Acad Sci USA 92:6224–6228PubMedGoogle Scholar
  79. Liesegang H, Lemke K, Siddiqui RA, Schlegel H-G (1993) Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 of Alcaligenes eutrophus CH34. J Bacteriol 175:767–778PubMedGoogle Scholar
  80. Lonetto M, Gribskov M, Gross CA (1992) The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol 174:3843–3849Google Scholar
  81. Lonetto MA, Brown KL, Rudd KE, Buttner MJ (1994) Analysis of the Streptomyces coelicolor sigF gene reveals the existence of a subfamily of eubacterial RNA polymerase σ factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci USA 91:7573–7577PubMedGoogle Scholar
  82. Maeda H, Jishage M, Ishihama A (2000a) Sigma competition: comparison of binding affinity to the core RNA polymerase among seven E. coli sigma subunits. Nucleic Acids Res 28:3497–3503CrossRefPubMedGoogle Scholar
  83. Maeda H, Jishage M, Nomura T, Fujita N, Ishihama A (2000b) Two extracytoplasmic function sigma subunits, σE and σFecI of Escherichia coli: promoter selectivity and intracellular levels. J Bacteriol 182:1181–1184CrossRefPubMedGoogle Scholar
  84. Mahren S, Braun V (2003) The FecI extracytoplasmic-function sigma factor of Escherichia coli interacts with the beta subunit of RNA polymerase. J Bacteriol 185:1796–1802CrossRefPubMedGoogle Scholar
  85. Majdalani N, Hernandez D, Gottesman S (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46:813–826CrossRefPubMedGoogle Scholar
  86. Manganelli R, Voskuil MI, Schoolnik GK, Smith I (2001) The Mycobacterium tuberculosis ECF sigma factor σE: role in global gene expression and survival in macrophages. Mol Microbiol 41:423–437CrossRefPubMedGoogle Scholar
  87. Manganelli R, Voskuil MI, Schoolnik GK, Dubnau E, Gomez M, Smith I (2002) Role of the extracytoplasmic-function sigma factor σH in Mycobacterium tuberculosis global gene expression. Mol Microbiol 45:365–374CrossRefPubMedGoogle Scholar
  88. Martinez-Bueno MA, Tobes R, Rey M, Ramos JL (2002) Detection of multiple extracytoplasmic function (ECF) sigma factors in the genome of Pseudomonas putida KT2440 and their counterparts in Pseudomonas aeruginosa PA01. Environ Microbiol 4:842–855CrossRefPubMedGoogle Scholar
  89. Minnig K, Barblan J-L, Kehl S, Möller SB, Mauël C (2003) In Bacillus subtilis W23, the duet sigmaXsigmaM, two sigma factors of the extracytoplasmic function subfamily, are required for septum and wall synthesis under batch culture conditions. Mol Microbiol 49:1435–1447CrossRefPubMedGoogle Scholar
  90. Missiakas D, Raina S (1998) The extracytoplasmic function sigma factors: role and regulation. Mol Microbiol 28:1059–1066Google Scholar
  91. Mittenhuber G (2002) An inventory of genes encoding RNA polymerase sigma factors in 31 completely sequenced eubacterial genomes. J Mol Microbiol Biotechnol 4:77–91PubMedGoogle Scholar
  92. Mouz S, Coursange E, Toussaint A (2001) Ralstonia metallidurans CH34 RpoN sigma factor and the control of nitrogen metabolism and biphenyl utilization. Microbiology Sgm 147:1947–1954Google Scholar
  93. Murakami KS, Masuda S, Campbell EA, Muzzin O, Darst SA (2002a) Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex. Science 296:1285–1290CrossRefPubMedGoogle Scholar
  94. Murakami KS, Masuda S, Darst SA (2002b) Structural basis of transcription initiation: RNA polymerase holoenzyme at a 4 Å resolution. Science 296:1280–1284CrossRefPubMedGoogle Scholar
  95. Narberhaus F (1999) Negative regulation of bacterial heat shock genes. Mol Microbiol 31:1–8PubMedGoogle Scholar
  96. Narberhaus F, Balsiger S (2003) Structure–function studies of Escherichia coli RpoH (σ32) by in vitro linker insertion mutagenesis. J Bacteriol 185:2731–2738CrossRefPubMedGoogle Scholar
  97. Navarro-Llorens JM, Martinez-Garcia E, Tormo A (2002) Enterobacter cloacae rpoS promoter and gene organization. Arch Microbiol 179:33–41CrossRefPubMedGoogle Scholar
  98. Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453PubMedGoogle Scholar
  99. Newman JD, Falkowski MJ, Schilke BA, Anthony LC, Donohue TJ (1999) The Rhodobacter sphaeroides ECF sigma factor, σE, and the target promoters cycA P3 and rpoE P1. J Mol Biol 294:307–320CrossRefPubMedGoogle Scholar
  100. Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339CrossRefPubMedGoogle Scholar
  101. Nies A, Nies DH, Silver S (1990) Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant from Alcaligenes eutrophus. J Biol Chem 265:5648–5653PubMedGoogle Scholar
  102. Notley-McRobb L, King T, Ferenci T (2002) rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J Bacteriol 184:806–811PubMedGoogle Scholar
  103. Paget MSB, Hong H-J, Bibb MJ, Buttner MJ (2002) The ECF sigma factors of Streptomyces coelicolor A3(2). In: Hodgson DA, Thomas CM (eds) SGM symposium 61: signals, switches, regulons and cascades: control of bacterial gene expression. Cambridge University Press, Cambridge, UKGoogle Scholar
  104. Pan Q, Losick R, Rudner DZ (2003) A second PDZ-containing serine protease contributes to activation of the sporulation transcription factor σK in Bacillus subtilis. J Bacteriol 185:6051–6056CrossRefPubMedGoogle Scholar
  105. Petersen L, Larsen TS, Ussery DW, On SLW, Krogh A (2003) RpoD promoters in Campylobacter jejuni exhibit a strong periodic signal instead of a-35 box. J Mol Biol 326:1361–1372CrossRefPubMedGoogle Scholar
  106. Pruteanu M, Hengge-Aronis R (2002) The cellular level of the recognition factor RssB is rate-limiting for σS proteolysis: implications for RssB regulation and signal transduction in σS turnover in Escherichia coli. Mol Microbiol 45:1701–1713CrossRefPubMedGoogle Scholar
  107. Raivio TL, Silhavy TJ (2001) Periplasmic stress and ECF sigma factors. Annu Rev Microbiol 55:591–624CrossRefPubMedGoogle Scholar
  108. Raj VS, Full C, Yoshida M, Sakata K, Kashiwagi K, Ishihama A, Igarashi K (2002) Decrease in cell viability in an RMF, sigma(38), and OmpC triple mutant of Escherichia coli. Biochem Biophys Res Commun 299:252–257CrossRefPubMedGoogle Scholar
  109. Reitzer L, Schneider BL (2001) Metabolic context and possible physiological themes of σ54-dependent genes in Escherichia coli. Microbiol Mol Biol Rev 65:422–444CrossRefPubMedGoogle Scholar
  110. Repoila F, Majdalani N, Gottesman S (2003) Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol Microbiol 48:855–861CrossRefPubMedGoogle Scholar
  111. Reyes-Dominguez Y, Contreras-Ferrat G, Ramirez-Santos J, Membrillo-Hernandez J, Gomez-Eichelmann MC (2003) Plasmid DNA supercoiling and gyrase activity in Escherichia coli wild-type and rpoS stationary-phase cells. J Bacteriol 185:1097–1100CrossRefPubMedGoogle Scholar
  112. Rezuchova B, Miticka H, Homerova D, Roberts M, Kormanec J (2003) New members of the Escherichia coli σE regulon identified by a two-plasmid system. FEMS Microbiol Lett 225:1–7CrossRefPubMedGoogle Scholar
  113. Robbe-Saule V, Algorta G, Rouilhac I, Norel F (2003) Characterization of the RpoS status of clinical isolates of Salmonella enterica. Appl Environ Microbiol 69:4352–4358CrossRefPubMedGoogle Scholar
  114. Ruiz N, Silhavy TJ (2003) Constitutive activation of the Escherichia coli pho regulon upregulates rpoS translation in an Hfq-dependent fashion. J Bacteriol 185:5984–5992CrossRefPubMedGoogle Scholar
  115. Samartzidou H, Delcour AH (1999) Excretion of endogenous cadaverine leads to a decrease in porin-mediated outer membrane permeability. J Bacteriol 181:791–798PubMedGoogle Scholar
  116. Sauer U, Santangelo JD, Treuner A, Buchholz M, Dürre P (1995) Sigma factor and sporulation genes in Clostridium. FEMS Microbiol Rev 17:331–340CrossRefPubMedGoogle Scholar
  117. Saumaa S, Tover A, Kasak L, Kivisaar M (2002) Different spectra of stationary-phase mutations in early-arising versus late-arising mutants of Pseudomonas putida: involvement of the DNA repair enzyme MutY and the stationary-phase sigma factor RpoS. J Bacteriol 184:6957–6965CrossRefPubMedGoogle Scholar
  118. Schmid AK, Lidstrom ME (2002) Involvement of two putative alternative sigma factors in stress response of the radioresistant bacterium Deinococcus radiodurans. J Bacteriol 184:6182–6189CrossRefPubMedGoogle Scholar
  119. Schmidt T, Schlegel HG (1994) Combined nickel–cobalt–cadmium resistance encoded by the ncc locus of Alcaligenes xylosoxidans 31A. J Bacteriol 176:7045–7054PubMedGoogle Scholar
  120. Schmidt-Eisenlohr H, Gast A, Baron C (2003) Inactivation of gacS does not affect the competitiveness of Pseudomonas chlororaphis in the Arabidopsis thaliana rhizosphere. Appl Environ Microbiol 69:1817–1826CrossRefPubMedGoogle Scholar
  121. Schnider-Keel U, Lejbølle KB, Baehler E, Haas D, Keel C (2001) The sigma factor AlgU (AlgT) controls exopolysaccharide production and tolerance towards desiccation and osmotic stress in the biocontrol agent Pseudomonas fluorescens CHA0. Appl Environ Microbiol 67:5683–5693CrossRefPubMedGoogle Scholar
  122. Shepherd NS, Churchward G, Bremer H (1980) Synthesis and activity of ribonucleic acid polymerase in Escherichia coli B/r. J Bacteriol 141:1098–1108PubMedGoogle Scholar
  123. Shepherd NS, Dennis P, Bremer E (2001) Cytoplasmic RNA polymerase in Escherichia coli. J Bacteriol 138:2527–2534CrossRefGoogle Scholar
  124. Silo-Suh L, Suh SJ, Sokol PA, Ohman DE (2002) A simple alfalfa seedling infection model for Pseudomonas aeruginosa strains associated with cystic fibrosis shows AlgT (sigma-22) and RhIR contribute to pathogenesis. Proc Natl Acad Sci USA 99:15699–15704CrossRefGoogle Scholar
  125. da Silva ACA, Simao RCG, Susin MF, Baidini RL, Avedissian M, Gomes SL (2003) Downregulation of the heat shock response is independent of DnaK and σ32 levels in Caulobacter crescentus. Mol Microbiol 49:541–553PubMedGoogle Scholar
  126. Soupene E, King N, Lee H, Kustu S (2002) Aquaporin Z of Escherichia coli: reassessment of its regulation and physiological role. J Bacteriol 184:4304–4307CrossRefPubMedGoogle Scholar
  127. Stiefel A, Mahren S, Ochs M, Schindler PT, Enz S, Braun V (2001) Control of the ferric citrate transport system of Escherichia coli: mutations in region 2.1 of the FecI extracytoplasmic-function sigma factor suppress mutations in the FecR transmembrane regulatory protein. J Bacteriol 183:162–170CrossRefPubMedGoogle Scholar
  128. Stragier P, Parsot C, Bouvier J (1985) Two functional domains conserved in major and alternate bacterial sigma factors. FEBS Lett 187:11–15CrossRefPubMedGoogle Scholar
  129. Studemann A, Noirclerc-Savoye M, Klauck E, Becker G, Schneider D, Hengge R (2003) Sequential recognition of two distinct sites in σS by the proteolytic targeting factor RssB and ClpX. EMBO J 22:4111–4120CrossRefPubMedGoogle Scholar
  130. Studholme DJ, Buck M, Nixon T (2000) Identification of potential N-dependent promoters in bacterial genomes. Microbiology (UK) 146:3021–3023Google Scholar
  131. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278:631–637PubMedGoogle Scholar
  132. Thackray PD, Moir A (2003) SigM, an extracytoplasmic function sigma factor of Bacillus subtilis, is activated in response to cell wall antibiotics, ethanol, heat, acid, and superoxide stress. J Bacteriol 185:3491–3498CrossRefPubMedGoogle Scholar
  133. Tibazarwa C, Wuertz S, Mergeay M, Wyns L, van der Lelie D (2000) Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J Bacteriol 182:1399–1409CrossRefPubMedGoogle Scholar
  134. Venturi V (2003) Control of rpoS transcription in Escherichia coli and Pseudomonas: why so different? Mol Microbiol 49:1–9CrossRefPubMedGoogle Scholar
  135. Viollier PH, Weihofen A, Folcher M, Thompson CJ (2003) Post-transcriptional regulation of the Streptomyces coelicolor stress responsive sigma factor, SigH, involves translational control, proteolytic processing, and an anti-sigma factor homolog. J Mol Biol 325:637–649CrossRefPubMedGoogle Scholar
  136. Visca P, Leoni L, Wilson MJ, Lamont IL (2002) Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45:1177–1190CrossRefPubMedGoogle Scholar
  137. Waterman SR, Small PLC (2003a) Identification of the promoter regions and σS-dependent regulation of the gadA and gadBC genes associated with glutamate-dependent acid resistance in Shigella flexneri. FEMS Microbiol Lett 225:155–160CrossRefPubMedGoogle Scholar
  138. Waterman SR, Small PLC (2003b) Transcriptional expression of Escherichia coli glutamate-dependent acid resistance genes gadA and gadBC in an hns rpoS mutant. J Bacteriol 185:4644–4647CrossRefPubMedGoogle Scholar
  139. Worhunsky DJ, Godek K, Litsch S, Schlax PJ (2003) Interactions of the non-coding RNA DsrA and RpoS mRNA with the 30 S ribosomal subunit. J Biol Chem 278:15815–15824CrossRefPubMedGoogle Scholar
  140. Wu J, Newton A (1997) The Caulobacter heat shock sigma factor gene rpoH is positively autoregulated from a σ32-dependent promoter. J Bacteriol 179:514–521PubMedGoogle Scholar
  141. Yoon SH, Han MJ, Lee SY, Jeong KJ, Yoo JS (2003) Combined transcriptome and proteome analysis of Escherichia coli during high cell density culture. Biotechnol Bioeng 81:753–767CrossRefPubMedGoogle Scholar
  142. Yoshida M, Kashiwagi K, Kawai G, Ishihama A, Igarashi K (2002) Polyamines enhance synthesis of the RNA polymerase σ38 subunit by suppression of an amber termination codon in the open reading frame. J Biol Chem 277:37139–37146CrossRefPubMedGoogle Scholar
  143. Zhang S, Haldenwang WG (2003) RelA is a component of the nutritional stress activation pathway of the Bacillus subtilis transcription factor σB. J Bacteriol 185Google Scholar
  144. Zuber U, Schumann W (1994) CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J Bacteriol 176:1359–1363PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Institut für MikrobiologieMartin-Luther-Universität Halle-WittenbergHalleGermany

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