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Volume 147, Issue 3

A role for DNA supercoiling in the regulation of the cytochrome oxidase of Free

Abstract

The operon of encodes cytochrome , a terminal oxidase in the aerobic respiratory chain. The high oxygen affinity of this oxidase explains its increased synthesis under low-oxygen conditions. Expression of the operon is controlled by the ArcA/ArcB two-component system and the oxygen-sensing transcriptional regulator Fnr. However, expression is still induced upon entry into stationary phase or following a shift to anaerobic conditions in a mutant deleted for and [Cotter, P. A. & Gunsalus, R. P. (1992), 91, 31–36]. Indeed, such a mutant contains 60% of the wild-type levels of spectrally detectable cytochrome . A possible mechanism to account for this regulation is that changes in negative supercoiling, which occur during a shift to low-oxygen or anaerobic conditions, may contribute to the regulation of the operon. This paper reports several lines of evidence in support of this idea. Firstly, the expression of , and the final level of spectrally detectable cytochrome , is sensitive to inhibitors of DNA gyrase, the enzyme responsible for introducing negative supercoils into DNA. Both nalidixic acid and novobiocin reduce expression in a concentration-dependent manner. Secondly, in a mutant, defective in DNA gyrase activity, expression of is reduced to a basal level that is no longer sensitive to the oxygen status. Both gyrase inhibitors and the mutation reduce expression in a strain deleted for and , indicating that their effects are not mediated indirectly through ArcA or Fnr, but rather that they are likely to be direct effects on expression. In conclusion, the authors have shown that changes in DNA supercoiling play a role in the induction of expression and may provide a general way of increasing cytochrome levels in the cell in response to environmental stress.

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Keyword(s): arcA , DNA gyrase , fnr , oxygen and respiration
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2001-03-01
2024-04-19
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References

  1. Atlung T., Brøndsted L. 1994; Role of the transcriptional activator AppY in regulation of the cyx appA operon of Escherichia coli by anaerobiosis, phosphate starvation, and growth phase. J Bacteriol 176:5414–5422
     [Google Scholar]
  2. Balke V. L., Gralla J. D. 1987; Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli . J Bacteriol 169:4499–4506
     [Google Scholar]
  3. Cotter P. A., Gunsalus R. P. 1992; Contribution of the fnr and arcA gene products in coordinate regulation of cytochrome o and d oxidases ( cyoABCDE and cydAB genes) in Escherichia coli . FEMS Microbiol Lett 91:31–36 [CrossRef]
     [Google Scholar]
  4. Cotter P. A., Chepuri V., Gennis R. B., Gunsalus R. P. 1990; Cytochrome o (cyoABCDE ) and d ( cydAB ) oxidase gene expression in Escherchia coli is regulated by oxygen, pH and the fnr gene product. J Bacteriol 172:6333–6338
     [Google Scholar]
  5. Cotter P. A., Melville S. B., Albrecht J. A., Gunsalus R. P. 1997; Aerobic regulation of cytochrome d oxidase ( cydAB ) operon expression in Escherichia coli : roles of Fnr and ArcA in repression and activation. Mol Microbiol 25:605–615 [CrossRef]
     [Google Scholar]
  6. Cunningham L., Williams H. D. 1995; Isolation and characterisation of mutants defective in the cyanide insensitive respiratory pathway of Pseudomonas aeruginosa . J Bacteriol 177:432–438
     [Google Scholar]
  7. Dassa E., Fsihi H., March C., Dion M., Kieffer-Bontemps M., Boquet P. L. 1991; 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 229:341–352 [CrossRef]
     [Google Scholar]
  8. Dimri G. P., Das H. K. 1988; Transcriptional regulation of nitrogen fixation genes by DNA supercoiling. Mol Gen Genet. 212360–363 [CrossRef]
  9. D’Mello R., Hill S., Poole R. K. 1996; The cytochrome bd quinol oxidase in Escherichia coli has an extremely high apparent affinity for oxygen and two oxygen-binding haems: implications for regulation of activity in vivo by substrate (oxygen) inhibition. Microbiology 142:755–763 [CrossRef]
     [Google Scholar]
  10. Dorman C. J. 1995; DNA topology and the global control of bacterial gene expression: implications for the regulation of virulence gene expression in pathogenic bacteria. Microbiology 141:1271–1280 [CrossRef]
     [Google Scholar]
  11. Dorman C. J., Barr G. C., Ni Bhriain N., Higgins C. F. 1988; DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression. J Bacteriol 179:2816–2826
     [Google Scholar]
  12. Drlica K. 1992; Control of bacterial DNA supercoiling. Mol Microbiol 6:425–433 [CrossRef]
     [Google Scholar]
  13. Drlica K., Coughlin S. 1989; Inhibitors of DNA gyrase. Pharmacol Ther 44:107–121 [CrossRef]
     [Google Scholar]
  14. Fisher L. M., Austin C. A., Hopewell R., Margerrison E. E. C., Oram M., Patel S., Plummer K., Sng J.-H., Sreedharan S. 1992; DNA supercoiling and relaxation by ATP-dependent DNA topoisomerases. Philos Trans R Soc Lond Ser B Biol Sci 336:83–91 [CrossRef]
     [Google Scholar]
  15. Garcı́a-Horsman J. A., Barquera B., Rumbley J., Ma J., Gennis R. B. 1994; The superfamily of haem–copper respiratory oxidases. J Bacteriol 176:5587–5600
     [Google Scholar]
  16. Gennis R. B., Stewart V. others 1996; Respiration. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology , 2nd edn. pp 217–261 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  17. Georgiou C. D., Dueweke T. J., Gennis R. B. 1988; Regulation of expression of cytochrome d of Escherichia coli is transcriptional. J Bacteriol 170:961–966
     [Google Scholar]
  18. Goldman B. S., Gabbert K. K., Kranz R. G. 1996; The temperature-sensitive growth and survival phenotypes of Escherichia coli cydDC and cydAB strains are due to deficiencies in cytochrome bd and are corrected by exogenous catalase and reducing agents. J Bacteriol 178:6348–6351
     [Google Scholar]
  19. Graeme-Cook K. A., May G., Bremer E., Higgins C. F. 1989; Osmotic regulation of porin expression: a role for DNA supercoiling. Mol Microbiol 3:1287–1294 [CrossRef]
     [Google Scholar]
  20. Grau R., Gardiol D., Gilkin G. C., di Mendoza D. 1994; DNA supercoiling and thermal regulation of unsaturated fatty acid synthesis in Bacillus subtilis . Mol Microbiol 11:933–941 [CrossRef]
     [Google Scholar]
  21. Green N. G., Fang H., Lin R.-J., Newton G., Mather M., Georgiou C., Gennis R. B. 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 263:13138–13143
     [Google Scholar]
  22. Hill J. J., Alben J. O., Gennis R. B. 1993; Spectroscopic evidence for a haem–haem binuclear center in the cytochrome bd ubiquinol oxidase from Escherichia coli . Proc Natl Acad Sci USA 90:5863–5867 [CrossRef]
     [Google Scholar]
  23. Iuchi S., Chepuri V., Fu H.-A., Gennis R. B., Lin E. C. C. 1990; Requirement for terminal cytochromes in generation of the aerobic signal for the arc regulatory system in Escherichia coli : study using deletions and lac fusions of cyo and cyd . J Bacteriol 172:6020–6025
     [Google Scholar]
  24. Junemann S. 1997; Cytochrome bd terminal oxidase. Biochim Biophys Acta 132:107–127
     [Google Scholar]
  25. Karem K., Foster J. W. 1993; The influence of DNA topology on the environmental regulation of a pH regulated locus in Salmonella typhimurium . Mol Microbiol 10:75–86 [CrossRef]
     [Google Scholar]
  26. Lorence R. M., Carter K., Green G. N., Gennis R. B. 1987; Cytochrome b -558 monitors the steady-state redox state of the ubiquinone pool in the aerobic respiratory chain of Escherichia coli . J Biol Chem 262:10532–10536
     [Google Scholar]
  27. Lynch A. S., Lin E. C. C. others 1996; Responses to molecular oxygen. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology , 2nd edn. pp 1526–1538 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  28. Markwell M. A. K., Haas S. M., Bieber L. L., Tolbert N. E. 1978; A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87:206–210 [CrossRef]
     [Google Scholar]
  29. Miller J. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  30. Miller M. J., Gennis R. B. 1983; The purification and characterisation of the cytochrome d terminal oxidase complex of the Escherichia coli aerobic respiratory chain. J Biol Chem 258:9159–9165
     [Google Scholar]
  31. Ni Bhriain N., Dorman C. J., Higgins C. F. 1989; An overlap between osmotic and anaerobic stress responses: a potential role for DNA supercoiling in the coordinate regulation of gene expression. Mol Microbiol 3:933–942 [CrossRef]
     [Google Scholar]
  32. O’Byrne C. P., Ni Bhriain N., Dorman C. J. 1992; The DNA sensitive supercoiling sensitive expression of the Salmonella typhimurium his operon requires the his attenuator and is modulated by anaerobiosis and by osmolarity. Mol Microbiol 6:2467–2476
     [Google Scholar]
  33. Poole R. K., Ingledew W. J. others 1987; Pathways of electrons to oxygen. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp 170–200 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  34. Poole R. K., Kumar C., Salmon I., Chance B. 1983; The 650 nm chromophore in Escherichia coli is an oxy-compound or oxygenated compound, not the oxidized form of cytochrome oxidase d – an hypothesis. J Gen Microbiol 129:1335–1344
     [Google Scholar]
  35. Poole R. K., Salmon I., Chance B. 1994; The high-spin cytochrome o ′ component of the cytochrome bo -type quinol oxidase in membranes from Escherichia coli : formation of the primary oxygenated species at low temperatures is characterized by a slow ‘on’ rate and low dissociation constant. Microbiology 140:1027–1034 [CrossRef]
     [Google Scholar]
  36. Pudek M. R., Bragg P. D. 1974; Inhibition by cyanide of the respiratory chain oxidases of Escherichia coli. Arch Biochem Biophys. 164682–693 [CrossRef]
  37. Rice C. W., Hempfling W. P. 1978; Oxygen-limited continuous culture and respiratory energy conservation in Escherichia coli . J Bacteriol 134:115–124
     [Google Scholar]
  38. Rothery R., Ingledew W. J. 1989; The cytochromes of anaerobically grown Escherichia coli . An electron paramagnetic study of the cytochrome bd complex in situ. Biochem J 262:437–443
     [Google Scholar]
  39. Schrum L. W., Hassan H. M. 1992; Transcriptional regulation of Mn-superoxide dismutase gene ( sodA ) of Escherichia coli is stimulated by DNA gyrase inhibitors. Arch Biochem Biophys 209:185–192
     [Google Scholar]
  40. Siegele D. A., Kolter R. 1993; Isolation and characterization of an Escherichia coli mutant defective in resuming growth after starvation. Genes Dev 7:2629–2640 [CrossRef]
     [Google Scholar]
  41. Siegele D. A., Imlay K. R., Imlay J. A. 1996; The stationary-phase-exit defect of cydC ( surB ) mutants is due to the lack of a functional terminal cytochrome oxidase. J Bacteriol 178:6091–6096
     [Google Scholar]
  42. Silhavy T. J., Berman M. L., Enquist L. W. 1984 Experiments with Gene Fusions Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  43. Sturr M. G., Krulwich T. A., Hicks D. B. 1996; Purification of a cytochrome bd terminal oxidase encoded by the Escherichia coli app locus from a Δ cyo Δ cyd strain complemented by genes from Bacilllus firmus OF4. J Bacteriol 176:1742–1749
     [Google Scholar]
  44. Sun L., Fuchs J. A. 1994; Regulation of the Escherichia coli nrd operon: role of DNA supercoiling. J Bacteriol 176:4617–4626
     [Google Scholar]
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A role for DNA supercoiling in the regulation of the cytochrome bd oxidase of Escherichia coli
Microbiology 147, 591 (2001); https://doi.org/10.1099/00221287-147-3-591
/content/journal/micro/10.1099/00221287-147-3-591
/content/journal/micro/10.1099/00221287-147-3-591
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