Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1994 Nov;176(21):6599–6605. doi: 10.1128/jb.176.21.6599-6605.1994

Effect of cell growth rate on expression of the anaerobic respiratory pathway operons frdABCD, dmsABC, and narGHJI of Escherichia coli.

C P Tseng 1, A K Hansen 1, P Cotter 1, R P Gunsalus 1
PMCID: PMC197015  PMID: 7961411

Abstract

The fumarate reductase (frdABCD), dimethyl sulfoxide (DMSO)-trimethylamine-N-oxide (TMAO) reductase (dmsABC), and nitrate reductase (narGHJI) operons in Escherichia coli encode enzymes involved in anaerobic respiration to the electron acceptors fumarate, DMSO or TMAO, and nitrate, respectively. They are regulated in response to anaerobiosis and nitrate availability. To determine how each operon is regulated in response to changes in cell growth rate and in oxygen availability, expression of frdA-lacZ, dmsA-lacZ, and narG-lacZ fusion genes was examined during continuous culture. After a change in the cell growth rate, each anaerobic electron transport pathway operon fusion responded somewhat differently. Whereas frdA-lacZ expression increased by fivefold as the growth rate decreased from 0.60 to 0.12/hour during aerobic growth, little change was seen under anaerobic conditions. In contrast, growth rate-dependent expression of narG-lacZ expression occurred under anaerobic conditions but not under aerobic conditions. Finally, dmsA-lacZ expression did not vary greatly for any of the growth rates tested. When cells were shifted from aerobic to anaerobic growth conditions, expression of each fusion increased at a moderate rate and peaked or "overshot" before reaching a new equilibrium value. This "overshoot" phenomenon was independent of the fnr gene product, which functions as a transcriptional activator of each respiratory operon during anaerobic conditions. In contrast to the moderate rate of anaerobic induction seen for narG-lacZ expression, the addition of nitrate caused a rapid induction response. The cell appears to have many ways to adjust cell respiration in response to changes in cell growth conditions.

Full text

PDF
6599

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 8. Microbiol Rev. 1990 Jun;54(2):130–197. doi: 10.1128/mr.54.2.130-197.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker H. V., 2nd, Wolf R. E., Jr Essential site for growth rate-dependent regulation within the Escherichia coli gnd structural gene. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7669–7673. doi: 10.1073/pnas.81.24.7669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bilous P. T., Weiner J. H. Molecular cloning and expression of the Escherichia coli dimethyl sulfoxide reductase operon. J Bacteriol. 1988 Apr;170(4):1511–1518. doi: 10.1128/jb.170.4.1511-1518.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chiang R. C., Cavicchioli R., Gunsalus R. P. Identification and characterization of narQ, a second nitrate sensor for nitrate-dependent gene regulation in Escherichia coli. Mol Microbiol. 1992 Jul;6(14):1913–1923. doi: 10.1111/j.1365-2958.1992.tb01364.x. [DOI] [PubMed] [Google Scholar]
  5. Cotter P. A., Chepuri V., Gennis R. B., Gunsalus R. P. Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. J Bacteriol. 1990 Nov;172(11):6333–6338. doi: 10.1128/jb.172.11.6333-6338.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cotter P. A., Darie S., Gunsalus R. P. The effect of iron limitation on expression of the aerobic and anaerobic electron transport pathway genes in Escherichia coli. FEMS Microbiol Lett. 1992 Dec 15;100(1-3):227–232. doi: 10.1111/j.1574-6968.1992.tb14045.x. [DOI] [PubMed] [Google Scholar]
  7. Cotter P. A., Gunsalus R. P. Oxygen, nitrate, and molybdenum regulation of dmsABC gene expression in Escherichia coli. J Bacteriol. 1989 Jul;171(7):3817–3823. doi: 10.1128/jb.171.7.3817-3823.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fowler A. V., Zabin I. Purification, structure, and properties of hybrid beta-galactosidase proteins. J Biol Chem. 1983 Dec 10;258(23):14354–14358. [PubMed] [Google Scholar]
  9. Grove C. L., Gunsalus R. P. Regulation of the aroH operon of Escherichia coli by the tryptophan repressor. J Bacteriol. 1987 May;169(5):2158–2164. doi: 10.1128/jb.169.5.2158-2164.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gunsalus R. P. Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. J Bacteriol. 1992 Nov;174(22):7069–7074. doi: 10.1128/jb.174.22.7069-7074.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jones H. M., Gunsalus R. P. Regulation of Escherichia coli fumarate reductase (frdABCD) operon expression by respiratory electron acceptors and the fnr gene product. J Bacteriol. 1987 Jul;169(7):3340–3349. doi: 10.1128/jb.169.7.3340-3349.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jones H. M., Gunsalus R. P. Transcription of the Escherichia coli fumarate reductase genes (frdABCD) and their coordinate regulation by oxygen, nitrate, and fumarate. J Bacteriol. 1985 Dec;164(3):1100–1109. doi: 10.1128/jb.164.3.1100-1109.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kalman L. V., Gunsalus R. P. The frdR gene of Escherichia coli globally regulates several operons involved in anaerobic growth in response to nitrate. J Bacteriol. 1988 Feb;170(2):623–629. doi: 10.1128/jb.170.2.623-629.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Metcalf W. W., Steed P. M., Wanner B. L. Identification of phosphate starvation-inducible genes in Escherichia coli K-12 by DNA sequence analysis of psi::lacZ(Mu d1) transcriptional fusions. J Bacteriol. 1990 Jun;172(6):3191–3200. doi: 10.1128/jb.172.6.3191-3200.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Meyer B. J., Schottel J. L. A novel transcriptional response by the cat gene during slow growth of Escherichia coli. J Bacteriol. 1991 Jun;173(11):3523–3530. doi: 10.1128/jb.173.11.3523-3530.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Miura A., Krueger J. H., Itoh S., de Boer H. A., Nomura M. Growth-rate-dependent regulation of ribosome synthesis in E. coli: expression of the lacZ and galK genes fused to ribosomal promoters. Cell. 1981 Sep;25(3):773–782. doi: 10.1016/0092-8674(81)90185-9. [DOI] [PubMed] [Google Scholar]
  17. Rabin R. S., Stewart V. Either of two functionally redundant sensor proteins, NarX and NarQ, is sufficient for nitrate regulation in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8419–8423. doi: 10.1073/pnas.89.18.8419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schröder I., Darie S., Gunsalus R. P. Activation of the Escherichia coli nitrate reductase (narGHJI) operon by NarL and Fnr requires integration host factor. J Biol Chem. 1993 Jan 15;268(2):771–774. [PubMed] [Google Scholar]
  19. Spiro S., Guest J. R. FNR and its role in oxygen-regulated gene expression in Escherichia coli. FEMS Microbiol Rev. 1990 Aug;6(4):399–428. doi: 10.1111/j.1574-6968.1990.tb04109.x. [DOI] [PubMed] [Google Scholar]
  20. Stewart V. Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol Rev. 1988 Jun;52(2):190–232. doi: 10.1128/mr.52.2.190-232.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Stewart V. Requirement of Fnr and NarL functions for nitrate reductase expression in Escherichia coli K-12. J Bacteriol. 1982 Sep;151(3):1320–1325. doi: 10.1128/jb.151.3.1320-1325.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Weiner J. H., MacIsaac D. P., Bishop R. E., Bilous P. T. Purification and properties of Escherichia coli dimethyl sulfoxide reductase, an iron-sulfur molybdoenzyme with broad substrate specificity. J Bacteriol. 1988 Apr;170(4):1505–1510. doi: 10.1128/jb.170.4.1505-1510.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES