Skip to main content
SpringerLink
Log in

Transcriptional Regulation by Nucleoid-Associated Proteins at Complex Promoters in Escherichia coli

  • Chapter
Bacterial Chromatin

Abstract

The expression of different Escherichia coli transcription units is tightly regulated at the level of transcription initiation. Promoter strength is fixed by DNA sequence elements, and changes in promoter activity are primarily modulated by a combination of sigma factors and transcription factors, whose activities are controlled by the growth environment. These factors all operate in the context of bacterial chromatin which plays a key role in the expression of many transcription units. Here we describe how IHF and FIS intervene directly at some complex Escherichia coli promoters to bring about different regulatory outcomes. At the nir operon promoter, the binding of IHF and FIS together makes expression co-dependent on two transcription activators that are triggered by two different environmental signals. We discuss three different mechanisms by which FIS represses promoter activity, thereby down-regulating gene expression during rapid growth. At the nrf operon promoter, FIS behaves as a conventional repressor, at the ogt and acs promoters, FIS displaces the essential activator, whilst, at the dps promoter, FIS jams RNA polymerase containing σ70 in an inactive complex. In each of the three cases, derepression occurs when FIS levels drop, as cell growth slows in response to nutrient limitation. Genomic studies of the distribution of IHF and FIS across the Escherichia coli chromosome suggest that they intervene at many intergenic regulatory regions, and that there may be little or no distinction between some nucleoid-associated proteins and transcription factors.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover 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

References

  • Almiron M, Link A, Furlong D, Kolter R (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6:1246-1254

    Article  Google Scholar 

  • Altuvia S, Almiron M, Huisman G, Kolter R, Storz G (1994) The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol Microbiol 13:265-272

    Article  CAS  PubMed  Google Scholar 

  • Ball C, Osuna R, Ferguson K, Johnson R (1992) Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J Bacteriol 174:8043-8056

    CAS  PubMed  Google Scholar 

  • Barnard A, Wolfe A, Busby S (2004) Regulation at complex bacterial promoters: how bacteria use different promoter organisations to produce different regulatory outcomes. Curr Opin Microbiol 7:102-108

    Article  CAS  PubMed  Google Scholar 

  • Beatty C, Browning D, Busby S, Wolfe A (2003) CRP-dependent activation of the Escherichia coli acsP2 promoter by a synergistic Class III mechanism. J Bacteriol 185:5148-5157

    Article  CAS  PubMed  Google Scholar 

  • Bell A, Cole J, Busby S (1990) Molecular genetic analysis of an FNR-dependent anaerobically-inducible Escherichia coli promoter. Mol Microbiol 4:1753-1763

    Article  CAS  PubMed  Google Scholar 

  • Brown N, Stoyanov J, Kidd S, Hobman J (2003) The MerR family of transcriptional regulators. FEMS Microbiol Rev 27:145-163

    Article  CAS  PubMed  Google Scholar 

  • Browning D, Busby S (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2:57-65

    Article  CAS  PubMed  Google Scholar 

  • Browning D, Cole J, Busby S (2000) Suppression of FNR-dependent transcription activation at the Escherichia coli nir promoter by Fis, IHF and H-NS: modulation of transcription initiation by a complex nucleo-protein assembly. Mol Microbiol 37:1258-1269

    Article  CAS  PubMed  Google Scholar 

  • Browning D, Lee D, Green J, Busby, S (2002a) Secrets of bacterial transcription initiation taught by the Escherichia coli FNR protein. In: Hodgson D, Thomas C (eds) Signals, switches, regulons and cascades: control of bacterial gene expression. SGM Symposium, volume 61, pp 127-142

    Google Scholar 

  • Browning D, Beatty C, Wolfe A, Cole J, Busby S (2002b) Independent regulation of the divergent nrfA and acsP1 Escherichia coli promoters by a nucleo-protein assembly at a shared regulatory region. Mol Microbiol 43:687-702

    Article  CAS  PubMed  Google Scholar 

  • Browning D, Cole J, Busby S (2004a) Transcription activation by remodeling of a nucleoprotein assembly: the role of NarL at the FNR-dependent Escherichia coli nir promoter. Mol Microbiol 53:203-215

    Article  CAS  PubMed  Google Scholar 

  • Browning D, Beatty C, Sanstad E, Gunn K, Busby S, Wolfe A (2004b) Modulation CRP-dependent transcription at the Escherichia coli acsP2 promoter: repression by the nucleoid proteins FIS and IHF. Mol Microbiol 51:241-254

    Article  CAS  PubMed  Google Scholar 

  • Browning D, Grainger D, Beatty C, Wolfe A, Cole J, Busby S (2005) Integration of three signals at the Escherichia coli nrf promoter: a role for Fis protein in catabolite repression. Mol Microbiol 57:496-510

    Article  CAS  PubMed  Google Scholar 

  • Browning D, Lee D, Wolfe A, Cole J, Busby S (2006) The Escherichia coli K-12 NarL and NarP proteins insulate the nrf promoter from the effects of integration host factor. J Bacteriol 188:7449-7456

    Article  CAS  PubMed  Google Scholar 

  • Browning D, Cole J, Busby S (2008) Regulation by nucleoid-associated proteins at the Escherichia coli nir operon promoter. J Bacteriol 190:7258-7267

    Article  CAS  PubMed  Google Scholar 

  • Busby S, Ebright R (1994) Promoter structure, promoter recognition and transcription activation in prokaryotes. Cell 79:743-746

    Article  CAS  PubMed  Google Scholar 

  • Cho B-K, Knight E, Barrett C, Palsson B (2008) Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res 18:900-910

    Article  CAS  PubMed  Google Scholar 

  • Choy H, Adhya S (1996) Negative control. In: Neidhardt F (ed) Escherichia coli and Salmonella, vol 1. ASM Press, Washington, DC, pp 1287-1299

    Google Scholar 

  • Constantinidou C, Hobman J, Griffiths L, Patel M, Penn C, Cole J, Overton T (2006) A reassessment of the FNR regulon and transcriptomic anakysis of the effects of nitrite, nitrate, NarXL, and NarQP as Escherichia coli K-12 adapts from aerobic to anaerobic growth. J Biol Chem 24:4802-4815

    Google Scholar 

  • Dame R (2005) The role of nucleoid-associated proteins in the organisation and compaction of bacterial chromatin. Mol Microbiol 56:858-870

    Article  CAS  PubMed  Google Scholar 

  • Finkel S, Johnson R (1992) The Fis protein: it’s not just for DNA inversion anymore. Mol Microbiol 6:3257-3265

    Article  CAS  PubMed  Google Scholar 

  • Grainger D, Busby S (2008) Methods for studying global patterns of DNA binding by bacterial transcription factors and RNA polymerase. Biochem Soc Trans 36:754-757

    Article  CAS  PubMed  Google Scholar 

  • Grainger D, Hurd D, Harrison M, Holdstock J, Busby S (2005) Studies of the distribution of Escherichia coli cAMP receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci USA 102:17693-17698

    Article  CAS  PubMed  Google Scholar 

  • Grainger D, Hurd D, Goldberg M, Busby S (2006) Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34:4642-4652

    Article  CAS  PubMed  Google Scholar 

  • Grainger D, Aiba H, Hurd D, Browning D, Busby S (2007) Transcription factor distribution in Escherichia coli: studies with FNR protein. Nucleic Acids Res 35:269-278

    Article  CAS  PubMed  Google Scholar 

  • Grainger D, Goldberg M, Lee D, Busby S (2008) Selective repression by Fis and H-NS at the E. coli dps promoter. Mol Microbiol 68:1366-1377

    Article  CAS  PubMed  Google Scholar 

  • Harborne N, Griffiths L, Busby S, Cole J (1992) Transcriptional control, translation and function of the products of the five open reading frames of the E. coli nir operon. Mol Microbiol 6:2805-2813

    Article  CAS  PubMed  Google Scholar 

  • Helmann J, Chamberlin M (1988) Structure and function of bacterial sigma factors. Ann Rev Biochem 57:839-872

    Article  CAS  PubMed  Google Scholar 

  • Hollands K, Busby S, Lloyd G (2007) New targets for the cyclic AMP receptor protein in the E. coli K-12 genome. FEMS Lett 274:89-94

    Article  CAS  Google Scholar 

  • Hussain H, Grove J, Griffiths L, Busby S, Cole J (1994) A seven gene operon essential for formate-dependent nitrite reduction to ammonia by enteric bacteria. Mol Microbiol 12:153-163

    Article  CAS  PubMed  Google Scholar 

  • Ishihama A (1997) Adaptation of gene expression in stationary phase bacteria. Curr Opin Gen Dev 7:582-588

    Article  CAS  Google Scholar 

  • Jayaraman S, Gaston K, Cole J, Busby S (1988) The nirB promoter of E. coli: location of nucleotide sequences essential for regulation by oxygen, the FNR protein and nitrite. Mol Microbiol 2:527-530

    Article  CAS  PubMed  Google Scholar 

  • Karp P, Keseler I, Shearer A, Latendresse M, Krummenacker M, Paley S, Paulsen I, Collado-Vides J, Gama-Castro S, Peralta-Gil M, Santos-Zavaleta A, Penaloza-Spinola M, Bonavides-Martinez C, Ingraham J (2007) Multidimensional annotation of the Escherichia coli K-12 genome. Nucleic Acids Res 35:7577-7590

    Article  CAS  PubMed  Google Scholar 

  • Kolb A, Spassky A, Chapon C, Blazy B, Buc H (1983) On the different binding affinities of CRP at the lac, gal and malT promoter regions. Nucleic Acids Res 11:7833-7852

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Bledsoe P, Stewart V (2007) Activation of yeaR-yoaG operon transcription by the nitrate-responsive regulator NarL is independent of oxygen-responsive regulator Fnr in Escherichia coli K-12. J Bacteriol 189:7539-7548

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Antonio A, Collado-Vides J (2003) Identifying global regulators in transcriptional regulatory networks in bacteria. Curr Opin Microbiol 6:482-489

    Article  CAS  PubMed  Google Scholar 

  • McLeod S, Johnson R (2001) Control of transcription by nucleoid proteins. Curr Opin Microbiol 4:152-159

    Article  CAS  PubMed  Google Scholar 

  • Miroslavova N, Busby S (2006) Investigations of the modular structure of bacterial promoters. Biochem Soc Symp 73:1-10

    CAS  PubMed  Google Scholar 

  • Murakami K, Darst S (2003) Bacterial RNA polymerases: the whole story. Curr Opin Struct Biol 13:31-39

    Article  CAS  PubMed  Google Scholar 

  • Ohniwa R, Morikawa K, Kim J, Ohta T, Ishihama A, Wada C, Takeyasu K (2006) Dynamic state of DNA topology is essential for genome condensation in bacteria. EMBO J 25:5591-5602

    Article  CAS  PubMed  Google Scholar 

  • Opel M, Aeling K, Holmes W, Johnson R, Benham C, Hatfield G (2004) Activation of transcription initiation from a stable RNA promoter by a Fis protein-mediated DNA structural transmission mechanism. Mol Microbiol 53:665-674

    Article  CAS  PubMed  Google Scholar 

  • Page L, Griffiths L, Cole J (1990) Differential physiological roles of two independent pathways for nitrite reduction to ammonia in enteric bacteria. Arch Microbiol 154:349-354

    Article  CAS  PubMed  Google Scholar 

  • Perez-Rueda E, Collado-Vides J (2000) The repertoire of DNA-binding transcriptional regulators in Escherichia coli K-12. Nucleic Acids Res 28:1838-1847

    Article  CAS  PubMed  Google Scholar 

  • Potter P, Wilkinson M, Fitton J, Carr F, Brennand J, Cooper D, Margeson G (1987) Characterisation and nucleotide sequence of ogt, the O6-alkylguanine-DNA-alkyl transferase of E. coli. Nucleic Acids Res 15:9177-9193

    Article  CAS  PubMed  Google Scholar 

  • Rhodius V, Busby S (1998) Positive activation of gene expression. Curr Opin Microbiol 1:152-159

    Article  CAS  PubMed  Google Scholar 

  • Richet E, Vidal-Ingigliardi D, Raibaud O (1991) A new mechanism for coactivation of transcription initiation: repositioning of an activator triggered by the binding of a second activator. Cell 66:1185-1195

    Article  CAS  PubMed  Google Scholar 

  • Robison K, McGuire A, Church G (1998) A comprehensive library of DNA-binding site matrices for 55 proteins applied to the complete Escherichia coli K-12 genome. J Mol Biol 284:241-254

    Article  CAS  PubMed  Google Scholar 

  • Rojo F (2001) Mechanisms of transcriptional repression. Curr Opin Microbiol 4:145-151

    Article  CAS  PubMed  Google Scholar 

  • Roy S, Dinitriadis E, Kar S, Geanacopoulos M, Lewis M, Adhya S (2005) Gal repressor-operator-HU ternary complex: pathway of repressosome formation. Biochemistry 44:5373-5380

    Article  CAS  PubMed  Google Scholar 

  • Saier M, Ramseier T (1996) The catabolite repressor/activator protein of bacteria. J Bacteriol 178:3411-3417

    CAS  PubMed  Google Scholar 

  • Samson L (1992) The suicidal DNA repair methyltransferases of bacteria. Mol Microbiol 6:825-831

    Article  CAS  PubMed  Google Scholar 

  • Schnetz K (2008) Fine-tuned growth control of dps, encoding a DNA protection protein, by FIS and H-NS. Mol Microbiol 68:1345-1347

    Article  CAS  PubMed  Google Scholar 

  • Schroder I, Darie S, Gunsalus R (1993) Activation of the Escherichia coli nitrate reductase (narGHJI) operon by NarL and FNR requires integration host factor. J Biol Chem 268:771-774

    CAS  PubMed  Google Scholar 

  • Schultz S, Shields G, Steitz T (1991) Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science 253:1001-1007

    Article  CAS  PubMed  Google Scholar 

  • Sclavi B, Beatty C, Thach D, Fredericks C, Buckle M, Wolfe A (2007) The multiple roles of CRP at the complex acs promoter depend on activation region 2 and IHF. Mol Microbiol 65:425-440

    Article  CAS  PubMed  Google Scholar 

  • Scott S, Busby S, Beacham I (1995) Transcriptional co-activation at the ansB promoters: involvement of the activating regions of CRP and FNR when bound in tandem. Mol Microbiol 18:521-531

    Article  CAS  PubMed  Google Scholar 

  • Semsey S, Virnik K, Adhya S (2005) A gamut of loops: meandering DNA. Trends Biochem Sci 30:334-341

    Article  CAS  PubMed  Google Scholar 

  • Sheridan S, Opel M, Hatfield G (2001) Activation and repression of transcription initiation by a distant DNA structural transition. Mol Microbiol 40:684-690

    Article  CAS  PubMed  Google Scholar 

  • Shimada T, Fujita N, Maeda M, Ishima A (2005) Systematic search for the Cra-binding promoters using genomic SELEX system. Genes Cells 10:907-918

    Article  CAS  PubMed  Google Scholar 

  • Shimada T, Ishihama A, Busby S, Grainger D (2008) The Escherichia coli RutR transcription factor binds at targets within genes as well as intergenic regions. Nucleic Acids Res 36:3950-3955

    Article  CAS  PubMed  Google Scholar 

  • Talukder A, Iwata A, Nishimura A, Ueda S, Ishihama A (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181:6361-6370

    Google Scholar 

  • Taverna P, Sedgwick B (1996) Generation of an endogenous DNA-methylating agent by nitrosation in Escherichia coli. J Bacteriol 178:5105-5111

    CAS  PubMed  Google Scholar 

  • Thanbichler M, Wang S, Shapiro L (2005) The bacterial nucleoid: a highly organized and dynamic structure. J Cell Biochem 96:506-521

    Article  CAS  PubMed  Google Scholar 

  • Tyson K, Bell A, Cole J, Busby S (1993) Identification of the nitrite and nitrate response elements at the anaerobically-inducible Escherichia coli nirB promoter. Mol Microbiol 7:151-157

    Article  CAS  PubMed  Google Scholar 

  • Tyson K, Cole J, Busby S (1994) Nitrite and nitrate regulation at the promoters of two Escherichia coli operons encoding nitrite reductase. Mol Microbiol 13:1045-1046

    Article  CAS  PubMed  Google Scholar 

  • Tyson K, Busby S, Cole J (1997) Catabolite regulation of two E. coli operons encoding nitrite reductases: role of Cra protein. Arch Microbiol 168:240-244

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Gunsalus R (2000) The nrfA and nirB nitrite reductase operons in Escherichia coli are expressed differentially in response to nitrate than to nitrite. J Bacteriol 182:5812-5823

    Google Scholar 

  • Weiss B (2006) Evidence for mutagenesis by nitric oxide during nitrate metabolism in Escherichia coli. J Bacteriol 188:829-833

    Article  CAS  PubMed  Google Scholar 

  • Wigneshweraraj S, Bose D, Burrows P, Joly N, Schumacher J, Rappas M, Pape T, Zheng X, Stockley P, Severinov K, Buck M (2008) Modus operandi of the bacterial RNA polymerase containing the sigma54 promoter-specificity factor. Mol Microbiol 69:538-546

    Article  Google Scholar 

  • Wing H, Williams S, Busby S (1995) Spacing requirements for transcription regulation by E. coli FNR protein. J Bacteriol 177:6704-6710

    CAS  PubMed  Google Scholar 

  • Wolfe A (2005) The acetate switch. Microbiol Mol Biol Rev 69:12-50

    Article  CAS  PubMed  Google Scholar 

  • Wu H-C, Tyson K, Cole J, Busby S (1998) Regulation of the E. coli nir operon by two transcription factors: a new mechanism to account for co-dependence on two activators. Mol Microbiol 27:493-505

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Work in the authors’ laboratory has been supported by the Wellcome Trust and the UK BBSRC.

Author information

Authors and Affiliations

  1. School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK

    Douglas F. Browning, David C. Grainger, Meng Xu & Stephen J. W. Busby

Authors
  1. Douglas F. Browning
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David C. Grainger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephen J. W. Busby
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen J. W. Busby .

Editor information

Editors and Affiliations

  1. Leiden Institute of Chemistry, Leiden University, Einsteinweg 55, 2333 CC, Leiden, Netherlands

    Remus T. Dame (Faculty of Mathematics and Natural Sciences) (Faculty of Mathematics and Natural Sciences)

  2. Division of Physics and Astronomy Section Physics of Complex Systems, VU University Amsterdam, De Boelelaan 1081, 1081 HV, Amsterdam, The Netherlands

    Remus T. Dame (Faculty of Mathematics and Natural Sciences) (Faculty of Mathematics and Natural Sciences)

  3. Department of Microbiology School of Genetics and Microbiology, University of Dublin Trinity College, Dublin 2, Ireland

    Charles J. Dorman

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Browning, D.F., Grainger, D.C., Xu, M., Busby, S.J.W. (2010). Transcriptional Regulation by Nucleoid-Associated Proteins at Complex Promoters in Escherichia coli . In: Dame, R.T., Dorman, C.J. (eds) Bacterial Chromatin. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3473-1_18

Download citation

Publish with us

Policies and ethics

Search

Navigation