Current Microbiology

, 33:270 | Cite as

Cooperative interaction between Cra and Fnr in the regulation of the cydAB operon of Escherichia coli

  • Tom M. Ramseier
  • Sharon Y. Chien
  • Milton H. Saier
Article

Abstract

In vivo and in vitro experiments are reported demonstrating that the catabolite repressoractivator (Cra) protein (formerly designated FruR) regulates expression of the cydAB operon of Escherichia coli encoding cytochrome d oxidase. The Fnr protein is required for Cra-mediated transcriptional control, but the ArcA protein antagonizes the response to Cra. The results establish that Fnr, ArcA, and Cra exert their effects in an interdependent fashion.

Literature Cited

  1. 1.
    Anraku Y, Gennis RB (1987) The aerobic respiratory chain of Escherichia coli. Trends Biochem Sci 12: 262–266CrossRefGoogle Scholar
  2. 2.
    Bates DM, Lazazzera BA, Kiley PJ (1995) Characterization of FNR* mutant proteins indicates two distinct mechanisms for altering oxygen regulation of the Escherichia coli transcription factor FNR. J Bacteriol 177: 3972–3978PubMedGoogle Scholar
  3. 3.
    Bledig SA, Ramseier TM, Saier MH Jr (1996) FruR mediates catabolite activation of pyruvate kinase (pykF) gene expression in Escherichia coli. J Bacteriol 178: 280–283PubMedGoogle Scholar
  4. 4.
    Chin AM, Feldheim DA, Saier MH Jr (1989) Altered transcriptional patterns affecting several metabolic pathways in strains of Salmonella typhimurium which overexpress the fructose regulon. J Bacteriol 171: 2424–2434PubMedGoogle Scholar
  5. 5.
    Compan I, Touati D (1994) Anaerobic activation of arcA transcription in Escherichia coli: roles of Fnr and ArcA. Mol Microbiol 11: 955–964PubMedCrossRefGoogle Scholar
  6. 6.
    Cotter PA, Gunsalus RP (1992) Contribution of the fnr and arcA gene products in coordinate regulation of cytochrome o and d oxidase (cyoABCDE and cydAB) genes in Escherichia coli. FEMS Microbiol Lett 91: 31–36CrossRefGoogle Scholar
  7. 7.
    Cotter PA, Chepuri V, Gennis RB, Gunsalus RP(1990) Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. J Bacteriol 172: 6333–6338PubMedGoogle Scholar
  8. 8.
    Cowell IG (1994) Repression versus activation in the control of gene transcription. Trends Biochem Sci 19: 38–42PubMedCrossRefGoogle Scholar
  9. 9.
    Fang H, Gennis RB (1993) Identification of the transcriptional start site of the cyd operon from Escherichia coli. FEMS Microbiol Lett 108: 237–242PubMedCrossRefGoogle Scholar
  10. 10.
    Fu H-A, Iuchi S, Lin ECC (1991) The requirement of ArcA and Fnr for peak expression of the cyd operon in Escherichia coli under microaerobic conditions. Mol Gen Genet 226: 209–213PubMedCrossRefGoogle Scholar
  11. 11.
    Georgiou CD, Dueweke TJ, Gennis RB (1988) Regulation of expression of the cytochrome d terminal oxidase in Escherichia coli is transcriptional. J Bacteriol 170: 961–966PubMedGoogle Scholar
  12. 12.
    Green GN, Fang H, Lin R-J, Newton G, Mather M, Georgiou CD, Gennis RB (1988) The nucleotide sequence of the cyd locus encoding the two subunits of the cytochrome d terminal oxidase complex of Escherichia coli. J Biol Chem 263: 13138–13143PubMedGoogle Scholar
  13. 13.
    Guarente L, Bermingham-McDonogh O (1992) Conservation and evolution of transcriptional mechanisms in eukaryotes. Trends Genet 8: 27–32PubMedCrossRefGoogle Scholar
  14. 14.
    Iuchi S, Lin ECC (1993) Adaptation of Escherichia coli to redox environments by gene expression. Mol Microbiol 9: 9–15PubMedCrossRefGoogle Scholar
  15. 15.
    Iuchi S, Chepuri V, Fu H-A, Gennis RB, Lin ECC (1990) Requirement for terminal cytochromes in generation of the aerobic signal for the arc regulatory system in Escherichia coli: study utilizing deletions and lac fusions of cyo and cyd. J Bacteriol 172: 6020–6025PubMedGoogle Scholar
  16. 16.
    Jones HM, Gunsalus RP (1987) Regulation of Escherichia coli fumarate reductase (frdABCD) operon expression by respiratory electron acceptors and the fnr gene product. J Bacteriol 169: 3340–3349PubMedGoogle Scholar
  17. 17.
    Kiley PJ, Reznikoff WS (1991) Fnr mutants that activate gene expression in the presence of oxygen. J Bacteriol 173: 16–22PubMedGoogle Scholar
  18. 18.
    Lazazzera BA, Bates DM, Kiley PJ (1993) The activity of the Escherichia coli transcription factor FNR is regulated by a change in oligomeric state. Genes Dev 7: 1993–2005PubMedCrossRefGoogle Scholar
  19. 19.
    Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor, New York: Cold Spring Harbor LaboratoryGoogle Scholar
  20. 20.
    Park S-J, Tseng C-P, Gunsalus RP (1995) Regulation of succinate dehydrogenase (sdhCDAB) operon expression in Escherichia coli in response to carbon supply and anaerobiosis: role of ArcA and Fnr. Mol Microbiol 15: 473–482PubMedCrossRefGoogle Scholar
  21. 21.
    Poole RK, Ingledew WJ (1987) Pathways of electrons to oxygen. In: Neidhardt FC (Editor in Chief) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. Washington, D.C.: American Society for Microbiology, pp 170–200Google Scholar
  22. 22.
    Pugh BF, Tjian R (1992) Diverse transcriptional functions of the multisubunit eukaryotic TFIID complex. J Biol Chem 267: 679–682PubMedGoogle Scholar
  23. 23.
    Ramseier TM (1996) Cra and the control of carbon flux via metabolic pathways. Res Microbiol, in pressGoogle Scholar
  24. 24.
    Ramseier TM, Saier MH Jr (1995) cAMP-cAMP receptor protein complex: five binding sites in the control region of the Escherichia coli mannitol operon. Microbiology 141: 1901–1907PubMedCrossRefGoogle Scholar
  25. 25.
    Ramseier TM, Nègre D, Cortay J-C, Scarabel M, Cozzone AJ, Saier MH Jr (1993) In vitro binding of the pleiotropic transcriptional regulatory protein, FruR, to the fru, pps, pts, icd and ace operons of Escherichia coli and Salmonella typhimurium. J Mol Biol 234: 28–44PubMedCrossRefGoogle Scholar
  26. 26.
    Ramseier TM, Bledig S, Michotey V, Feghali R, Saier MH Jr (1995) The global regulatory protein, FruR, modulates the direction of carbon flow in enteric bacteria. Mol Microbiol 16: 1157–1169PubMedCrossRefGoogle Scholar
  27. 27.
    Ryu S, Ramseier TM, Michotey V, Saier MH Jr, Garges S (1995) Effect of the FruR regulator on transcription of the pts operon in Escherichia coli. J Biol Chem 270: 2489–2496PubMedCrossRefGoogle Scholar
  28. 28.
    Saier MH Jr (1985) Mechanisms and regulation of carbohydrate transport in bacteria. New York, N.Y.: Academic PressGoogle Scholar
  29. 29.
    Saier MH Jr, Chin M (1990) Energetics of the bacterial phosphotransferase system in sugar transport and the regulation of carbon metabolism. In: Krulwich TA (ed) Bacterial energetics (A volume in The bacteria: a treatise on structure and function). New York: Academic Press, pp 273–299Google Scholar
  30. 30.
    Saier MH Jr, Ramseier TM (1996) The catabolite repressor/ activator (Cra) protein of enteric bacteria. J Bacteriol 178: 3411–3417PubMedGoogle Scholar
  31. 31.
    Sawers G, Suppmann B (1992) Anaerobic induction of pyruvate formate-lyase gene expression is mediated by the ArcA and FNR proteins. J Bacteriol 174: 3474–3478PubMedGoogle Scholar
  32. 32.
    Spiro S, Guest JR (1990) FNR and its role in oxygen-regulated gene expression in Escherichia coli. FEMS Microbiol Rev 75: 399–428CrossRefGoogle Scholar
  33. 33.
    Tardat B, Touati D (1993) Iron and oxygen regulation of Escherichia coli MnSOD expression: Competition between the global regulators Fur and ArcA for binding to DNA. Mol Microbiol 9: 53–63PubMedCrossRefGoogle Scholar
  34. 34.
    Ziegelhoffer EC, Kiley PJ (1995) In vitro analysis of a constitutively active mutant form of the Escherichia coli global transcription factor FNR. J Mol Biol 245: 351–361PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Tom M. Ramseier
    • 1
  • Sharon Y. Chien
    • 1
  • Milton H. Saier
    • 1
  1. 1.Department of BiologyUniversity of California at San DiegoLa JollaUSA

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