Skip to main content
SpringerLink
Log in

Regulation of Gene Expression in Stationary Phase

  • Chapter
Regulation of Gene Expression in Escherichia coli

Abstract

Among the first concepts presented to a student of microbiology is the simplified view of the phases of a bacterial culture: lag, exponential, and stationary. Interest in studying the underlying physiology of a bacterial cell as it shifts between these phases has always been high among bacterial physiologists. Despite this interest, molecular genetic approaches were not applied to the study of regulation of gene expression in stationary phase Escherichia coli cultures until the last few years. This may have been partially due to the fact that many investigators felt that, in contrast to the highly differentiated spores of starving Bacillus subtilis, 1 Myxococcus xanthus, 2 or Streptomyces, 3 starved E. coli cells were simply a nongrowing version of exponential phase cells. The fact that microorganisms in nature must by necessity spend most of their existence in a nongrowing, or an extremely slow growing state, eventually led some investigators to the study of nongrowing E. coli in the laboratory. As more and more researchers explore the E. coli starvation response we are beginning to understand the remarkable developmental changes this organism undergoes during stationary phase.4-7 Cells respond to starvation by turning on a reversible program of gene expression enabling them to survive prolonged periods of nutrient deprivation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Losick R, Stragier P. Crisscross regulation of cell-type-specific gene expression during development in B. subtilis. Nature 1992; 355:601–604.

    Article  Google Scholar 

  2. Kim SK, Kaiser D, Kuspa A. Control of cell density and pattern by intercellular signaling in Myxococcus development. Annu Rev Microbiol 1992; 46:117–139.

    Article  Google Scholar 

  3. Chater KF. Genetics of differentiation in Streptomyces. Annu Rev Microbiol 1993; 47:685–713.

    Article  Google Scholar 

  4. Matin A. The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol Microbiol 1991; 5:3–10.

    Article  Google Scholar 

  5. Hengge-Aronis R. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in Escherichia coli. Cell 1993; 72:165–168.

    Article  Google Scholar 

  6. Huisman G, Kolter R. Regulation of gene expression at the onset of stationary phase in Escherchia coli. In: Piggot P, Moran C, Youngman P, eds. Regulation of Bacterial Differentiation. Washington, DC: American Society for Microbiology, 1993:21–40.

    Google Scholar 

  7. Kolter R, Siegele DA, Tormo A. The Stationary Phase of the Bacterial Life Cycle. Ann Rev Microbiol 1993; 47:855–874.

    Article  Google Scholar 

  8. Giaever HM, Styrvold OB, Kaasen I et al. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. J Bacteriol 1988; 170:2841–2849.

    Google Scholar 

  9. Kaasen I, Falkenberg P, Styrvold OB et al. Molecular cloning and physical mapping of the otsAB genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: Evidence that transcription is activated by KatF (AppR). J Bacteriol 1992; 174:889–898.

    Google Scholar 

  10. Loewen PC, Triggs BL. Genetic mapping of katF, a locus that with katE affects the synthesis of a second catalase species in Escherichia coli. J Bacteriol 1984; 160:668–675.

    Google Scholar 

  11. Sak BD, Eisenstark A, Touati D. Exonuclease III and the hydroperoxidase II in Escherichia coli are both regulated by the katF product. Proc Natl Acad Sci USA 1989; 86:3271–3275.

    Article  Google Scholar 

  12. Almirón M, Link A, Furlong D et al. A novel DNA binding protein with regulatory and protective roles in starved E. coli. Genes Dev 1992; 6:2646–2654.

    Article  Google Scholar 

  13. Jenkins DE, Auger EA, Matin A. Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival. J Bacteriol 1991; 173:1992–1996.

    Google Scholar 

  14. Preiss J. Bacterial glycogen synthesis and its regulation. Ann Rev Microbiol 1984; 38:419–458.

    Article  Google Scholar 

  15. Damotte M, Cattaneo J, Sigal N et al. Mutants oí Escherichia coli K12 altered in their ability to store glycogen. Biochem Biophys Res Comm 1968; 32:916–920.

    Article  Google Scholar 

  16. Crooke E, Akiyama M, Rao NN et al. Genetically altered levels of inorganic polyphosphate in Escherichia coli. J Biol Chem 1994; 269:6290–6295.

    Google Scholar 

  17. Ivanov AI, Fomchenkov VM. Relation between the damaging effect of surface-active compounds on Escherichia coli cells and the phase of culture growth. Mikrobiologiia 1989; 58:969–975.

    Google Scholar 

  18. Wensink J, Gilden N, Witholt B. Attachment of lipoprotein to the murein of Escherichia coli. Eur J Biochem 1982; 122:587–590.

    Article  Google Scholar 

  19. Pisabarro AG, de Pedro MA, Vazquez D. Structural modifications in the peptidoglycan of Escherichia coli associated with changes in the state of growth of the culture. J Bacteriol 1985; 161:238–242.

    Google Scholar 

  20. Groat RG, Schultz JE, Zychlinsky E et al. Starvation proteins in Escherichia coli: Kinetics of synthesis and role in starvation survival. J Bacteriol 1986; 168:486–493.

    Google Scholar 

  21. Lange R, Hengge-Aronis R. Identification of a central regulator of stationary phase gene expession in E. coli. Mol Microbiol 1991; 5:49–59.

    Article  Google Scholar 

  22. Romeo T, Preiss J. Genetic regulation of glycogen biosynthesis in Escherichia coli. In vitro effects of cyclic AMP and guanosine 5’-diphosphate 3’-diphosphate and analysis of in vivo transcripts. J Bacteriol 1989; 171:2773–2782.

    Google Scholar 

  23. Okita T, Rodriguez R, Preiss J. Biosynthesis of bacterial glycogen. J Biol Chem 1981; 256:6944–6952.

    Google Scholar 

  24. Schultz JE, Matin A. Molecular and functional characterization of a carbon starvation gene of Escherichia coli. J Mol Biol 1991; 218:129–140.

    Article  Google Scholar 

  25. Hernandez-Chico C, San Millan JL, Kolter R et al. Growth phase and OmpR regulation of transcription of the Microcin B17 genes. J Bacteriol 1986; 167:1058–1065.

    Google Scholar 

  26. McCann MP, Kidwell JP, Matin A. The putative σ factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J Bacteriol 1991; 173:4188–4194.

    Google Scholar 

  27. Lange R, Hengge-Aronis R. Growth phase-regulated expression of bolA and morphology of stationary phase Escherichia coli cells is controlled by the novel sigma factor σs (rpoS). J Bacteriol 1991; 173:4474–4481.

    Google Scholar 

  28. Touati E, Dassa E, Boquet PL. Pleiotropic mutations in appR reduce pH 2.5 acid phosphatase expression and restore succinate utilization in CRP-deficient strains of Escherichia coli. Mol Gen Genet 1986; 202:257–264.

    Article  Google Scholar 

  29. Tuveson RW. The interaction of a gene (nur) controlling near-UV sensitivity and the polA1 gene in strains of E. coli K-12. Photochem Photobiol 1981; 33:919–923.

    Article  Google Scholar 

  30. Mulvey MR, Loewen PC. Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel transcription factor. Nucleic Acids Res 1989; 17:9979–9991.

    Article  Google Scholar 

  31. Ding Q, Kusano S, Villarejo M et al. Promoter selectivity control of Escherichia coli RNA polymerase by ionic strength: differential recognition of osmoregulated promoters by EσD and Eσs holoenzymes. Mol Microbiol 1995; 16:649–656.

    Article  Google Scholar 

  32. Nguyen LH, Jensen DB, Thompson NE et al. In vitro functional characterization of overproduced Escherichia coli katF/rpoS gene product. Biochemistry 1993; 32:11112–1117.

    Article  Google Scholar 

  33. Tanaka K, Takayanagi Y, Fujita N et al. Heterogeneity of the principal sigma factor in Escherichia coli: the rpoS gene product, σ38, is a principal sigma factor of RNA polymerase in stationary phase Escherichia coli. Proc Natl Acad Sci USA 1993; 90:3511–3515.

    Article  Google Scholar 

  34. Weichart D, Lange R, Henneberg N et al. Identification and characterization of stationary phase-inducible genes in Escherichia coli. Mol Microbiol 1993; 10:407–420.

    Article  Google Scholar 

  35. Hengge-Aronis R, Klein W, Lange R et al. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary phase thermotolerance in Escherichia coli. J Bacteriol 1991; 173:7918–7924.

    Google Scholar 

  36. Loewen PC, Switala J, Triggs-Raine BL. Catalase HPI and HPII in Escherichia coli are induced independently. Arch Biochem Biophys 1985; 243:144–149.

    Article  Google Scholar 

  37. Hengge-Aronis R, Fischer D. Identification and molecular analysis of glgS, a novel growth-phase-regulated and rpoS-dependent gene involved in glycogen synthesis in Escherichia coli. Mol Microbiol 1992; 6:1877–1886.

    Article  Google Scholar 

  38. Wang A-Y, Cronan JE. The growth phase-dependent synthesis of cyclopropane fatty acids in Escherichia coli is the result of an RpoS (KatF)-dependent promoter plus enzyme instability. Mol Microbiol 1994; 11:1009–1017.

    Article  Google Scholar 

  39. Begg KJ, Takasuga A, Edwards DH et al. The balance between different peptidoglycan precursors determines whether Escherichia coli cells will elongate or divide. J Bacteriol 1990; 172:6697–6703.

    Google Scholar 

  40. Dougherty TJ, Pucci MJ. Penicillin-binding proteins are regulated by rpoS during transitions in growth states of Escherichia coli. Antimicrob Agents Chemother 1994; 1994:205–210.

    Google Scholar 

  41. Atlung T, Nielsen A, Hansen FG. Isolation, characterization, and nucleotide sequence of appY, a regulatory gene for growth-phase-dependent gene expression in Escherichia coli. J Bacteriol 1989; 171:1683–1691.

    Google Scholar 

  42. Dassa J, Fsihi H, Marck C et al. A new oxygen-regulated operon in Escherichia coli comprises the genes for a putative third cytochrome oxidase and for pH 2.5 acid phosphatase (appA). Mol Gen Genet 1992; 229:342–352.

    Google Scholar 

  43. Brøndsted L, Atlung T. Anaerobic regulation of the hydrogenase 1 (hya) operon of Escherichia coli. J Bacteriol 1994; 176:5423–5428.

    Google Scholar 

  44. Aldea M, Garrido T, Pla J et al. Division genes in Escherichia coli are expressed coordinately to cell septum requirements by gearbox promoters. EMBO J 1990; 9:3787–3794.

    Google Scholar 

  45. Bohannon DE, Connell N, Keener J et al. Stationary-phase-inducible “gearbox” promoters: differential effects of katF mutations and the role of σ70. J Bacteriol 1991; 173:4482–4492.

    Google Scholar 

  46. Vicente M, Kushner SR, Garrido T et al. The role of the “gearbox” in the transcription of essential genes. Mol Microbiol 1991; 5:2085–2091.

    Article  Google Scholar 

  47. Higgins CF, Dorman CJ, Stirling DA et al. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 1988; 52:569–584.

    Article  Google Scholar 

  48. Espinosa-Urgel M, Tormo A. Sigma a-dependent promoters in Escherichia coli are located in DNA regions with intrinsic curvature. Nuc Acids Res 1993; 21:3667–3670.

    Article  Google Scholar 

  49. Altuvia S, Almirón M, Huisman G et al. The dps promoter is activated by OxyR during growth and by IHF and σ s in stationary phase. Mol Microbiol 1994; 13:265–272.

    Article  Google Scholar 

  50. Lange R, Barth M, Hengge-Aronis R. Complex transcriptional control of the σ-s dependent stationary-phase-induced and osmotically regulated osmY (csi-5) gene suggests novel roles for Lrp, cyclic AMP (cAMP) receptor protein-cAMP complex, and integration host factor in the stationary-phase response of Escherichia coli. J Bacteriol 1993; 175:7910–7917.

    Google Scholar 

  51. Olsén A, Arnqvist A, Sukupolvi S et al. The RpoS sigma factor relieves H-NS mediated transcriptional repression of csgA, the subunit gene of fibronectin binding curli in Escherichia coli. Mol Microbiol 1993; 7:523–536.

    Article  Google Scholar 

  52. Ozaki M, Wada A, Fujita N et al. Growth phase-dependent modification of RNA polymerase in Escherichia coli. Mol Gen Genet 1991; 230:17–23.

    Article  Google Scholar 

  53. Mulvey MR, Switala J, Borys A et al. Regulation of transcription of katE and katF in Escherichia coli. J Bacteriol 1990; 172:6713–6720.

    Google Scholar 

  54. Schellhorn HE, Stones VL. Regulation of katF and katE in Escherichia coli K-12 by weak acids. J Bacteriol 1992; 174:4769–4776.

    Google Scholar 

  55. Lange R, Hengge-Aronis R. The nlpD gene is located in an Operon with rpoS on the Escherichia coli chromosome and encodes a novel lipoprotein with a potential function in cell wall formation. Mol Microbiol 1994; 13:733–743.

    Article  Google Scholar 

  56. Takayanagi Y, Tanaka K, Takahashi H. Structure of the 5’ upstream region and the regulation of the rpoS gene of Escherichia coli. Mol Gen Genet 1994; 243:525–531.

    Article  Google Scholar 

  57. Ichikawa JK, Li C, Fu J et al. A gene at 59 minutes on the Escherichia coli chromosome encodes a lipoprotein with unusual amino acid repeat sequences. J Bacteriol 1994; 176:1630–1638.

    Google Scholar 

  58. Lange R, Hengge-Aronis R. The cellular concentration of the σ s subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev 1994; 8:1600–1612.

    Article  Google Scholar 

  59. Gentry DR, Hernández VJ, Nguyen LH et al. Synthesis of the stationary-phase sigma factor, σs, is positively regulated by ppGpp. J Bacteriol 1993; 175:7982–7989.

    Google Scholar 

  60. Vogel U, Sørensen M, Pedersen S et al. Decreasing transcription elongation rate in Escherichia coli exposed to amino acid starvation. Mol Microbiol 1992; 6:2191–2200.

    Article  Google Scholar 

  61. Faxen M, Isaksson LA. Functional interactions between translation, transcription and ppGpp in growing Escherichia coli. Biochim Biophys Acta 1994; 1219:425–434.

    Google Scholar 

  62. Huisman GW, Kolter R. Sensing starvation: a homoserine lactone-depen-dent signaling pathway in Escherichia coli. Science 1994; 265:537–539.

    Article  Google Scholar 

  63. Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 1994; 176:269–275.

    Google Scholar 

  64. Engebrecht J, Nealson K, Silverman M. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 1983; 32:773–781.

    Article  Google Scholar 

  65. Wang X, deBoer PAJ, Rothfield LI. A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division genes of Escherichia coli. EMBO J 1991; 10:3363–3372.

    Google Scholar 

  66. Loewen PC, von Ossowski I, Switala J et al. Regulation of KatF synthesis in Escherichia coli. J Bacteriol 1993; 175:2150–2153.

    Google Scholar 

  67. McCann MP, Fraley CD, Matin A. The putative a factor KatF is regulated post-transcriptionally during carbon starvation. J Bacteriol 1993; 175:2143–2149.

    Google Scholar 

  68. Bohringer J, Fischer D, Mosler G et al. UDP-glucose is a potential intracellular signal molecule in the control of expression of σs and σs-dependent genes in Escherichia coli. J Bacteriol 1995; 177:413–422.

    Google Scholar 

  69. Yamashino T, Ueguchi C, Mizuno T. Quantitative control of the stationary phase-specific sigma factor, σs, in Escherichia coli: involvement of the nucleoid protein H-NS. EMBO J 1995; 14:594–602.

    Google Scholar 

  70. Bosl M, Kersten H. Organization and functions of genes in the upstream region of tyrT of Escherichia coli: phenotypes of mutants with partial deletion of a new gene (tgs). J Bacteriol 1994; 176:221–231.

    Google Scholar 

  71. Hengge-Aronis R, Lange R, Henneberg N et al. Osmotic regulation of rpoS-dependent genes in Escherichia coli. J Bacteriol 1993; 175:259–265.

    Google Scholar 

  72. Zambrano MM, Siegele DA, Almirón M et al. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 1993; 259:1757–1760.

    Article  Google Scholar 

  73. Yamashino T, Kakeda M, Ueguchi C et al. An analog of the DnaJ molecular chaperone whose expression is controlled by σs during the stationary phase and phosphate starvation in Escherichia coli. Mol Microbiol 1994; 13:475–483.

    Article  Google Scholar 

  74. Mukhopadhyay S, Schellhorn HE. Induction of Escherichia coli hydro-peroxidase I by acetate and other weak acids. J Bacteriol 1994; 176:2300–2307.

    Google Scholar 

  75. Aldea M, Garrido T, Hernández-Chico C et al. Induction of a growth-phase-dependent promoter triggers transcription of bolA, an E. coli morphogene. EMBO J 1989; 8:3923–3931.

    Google Scholar 

  76. Kawamukai M, Matsuda H, Fujii W et al. Cloning of the fic-1 gene involved in cell filamentation induced by cyclic AMP and construction of a Δfic Escherichia coli strain. J Bacteriol 1988; 170:3864–3869.

    Google Scholar 

  77. Boos W, Ehmann U, Bremer E et al. Trehalase of Escherichia coli. J Biol Chem 1987; 262:13212–13218.

    Google Scholar 

  78. Raina S, Missiakis D, Baird L et al. Identification and transcriptional analysis of the Escherichia coli htrE Operon which is homologous to pap and related pili operons. J Bacteriol 1993; 175:5009–5021.

    Google Scholar 

  79. Jung JU, Gutierrez C, Martin F et al. Transcription of osmB, a gene encoding an Escherichia coli lipoprotein, is regulated by dual signals. J Biol Chem 1990; 265:10574–10581.

    Google Scholar 

  80. Magnuson K, Jackowski S, Rock CO et al. Regulation of fatty acid biosynthesis in Escherichia coli. Microbiol Rev 1993; 57:522–542.

    Google Scholar 

  81. Yang CC, Konisky J. Colicin V-treated Escherichia coli does not generate membrane potential. J Bacteriol 1984; 158:757–759.

    Google Scholar 

  82. Diaz-Guerra L, Moreno F, SanMillan JL. appR gene product activates transcription of microcin C7 plasmid genes. J Bacteriol 1989; 171: 2906–2908.

    Google Scholar 

  83. Chang Y-Y, Wang A-Y, Cronan JE. Expression of Escherichia coli pyruvate oxidase (PoxB) depends on the sigma factor encoded by the rpoS(katF) gene. Mol Microbiol 1994; 11:1019–1028.

    Article  Google Scholar 

  84. Mellies J, Wise A, Villarejo M. Two different Escherichia coli proP promoters respond to osmotic and growth phase signals. J Bacteriol 1995; 177:144–151.

    Google Scholar 

  85. Xu J, Johnson RC. aldB, an RpoS-dependent gene in Escherichia coli encoding an aldehyde dehydrogenase that is repressed by Fis and activated by Crp. J Bacteriol 1995; 177:3166–3175.

    Google Scholar 

Download references

Authors
  1. Heidi Goodrich-Blair
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María Uría-Nickelsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roberto Kolter
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 1996 R.G. Landes Company

About this chapter

Cite this chapter

Goodrich-Blair, H., Uría-Nickelsen, M., Kolter, R. (1996). Regulation of Gene Expression in Stationary Phase. In: Regulation of Gene Expression in Escherichia coli . Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-8601-8_27

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-8601-8_27

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-8603-2

  • Online ISBN: 978-1-4684-8601-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation