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. 1986 Dec;168(3):1415–1421. doi: 10.1128/jb.168.3.1415-1421.1986

Three classes of Escherichia coli mutants selected for aerobic expression of fumarate reductase.

S Iuchi, D R Kuritzkes, E C Lin
PMCID: PMC213654  PMID: 3536878

Abstract

Fumarate reductase (encoded by frd) and succinate dehydrogenase (encoded by sdh) of Escherichia coli are both known to catalyze the interconversion of fumarate and succinate. Fumarate reductase, however, is not inducible aerobically and therefore cannot participate in the dehydrogenation of succinate. Three classes of suppressor mutants, classified as frd oxygen-resistant [frd(Oxr)], constitutive [frd(Con)], and gene amplification [frd(Amp)] mutants, were selected from an sdh strain as pseudorevertants that regained the partial ability to grow aerobically on succinate. All contained increased aerobic levels of fumarate reductase activity. In frd(Oxr) mutants expression of the operon showed increased resistance to aerobic repression. Under anaerobic conditions expression of the operon became less dependent on the fnr+ gene product, a pleiotropic activator protein for genes encoding anaerobic respiratory enzymes. Exogenous fumarate, however, was still required for full induction, and repression by nitrate was undiminished. Thus, aerobic repression and anaerobic nitrate repression appear to involve separate mechanisms. In frd(Con) mutants expression of the operon became highly resistant to aerobic repression. Under anaerobic conditions expression of the operon no longer required the fnr+ gene product or exogenous fumarate and became immune to nitrate repression. In partial diploids bearing an frd(Oxr) or an frd(Con) allele and phi(frd+-lac) there was no mutual regulatory influence between the two genetic loci. Thus, the frd mutations act in cis and hence are probably in the promoter region. In frd(Amp) mutants the frd locus was amplified without significant alteration in the pattern of regulation.

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Selected References

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  1. Burman L. G., Park J. T., Lindström E. B., Boman H. G. Resistance of Escherichia coli to penicillins: identification of the structural gene for the chromosomal penicillinase. J Bacteriol. 1973 Oct;116(1):123–130. doi: 10.1128/jb.116.1.123-130.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. COHN M., HORIBATA K. Inhibition by glucose of the induced synthesis of the beta-galactoside-enzyme system of Escherichia coli. Analysis of maintenance. J Bacteriol. 1959 Nov;78:601–612. doi: 10.1128/jb.78.5.601-612.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chippaux M., Bonnefoy-Orth V., Ratouchniak J., Pascal M. C. Operon fusions in the nitrate reductase operon and study of the control gene nir R in Escherichia coli. Mol Gen Genet. 1981;182(3):477–479. doi: 10.1007/BF00293938. [DOI] [PubMed] [Google Scholar]
  4. Chippaux M., Giudici D., Abou-Jaoudé A., Casse F., Pascal M. C. Laboratoire de Chimie Bactérienne C.N.R.S., Marsielle, France. Mol Gen Genet. 1978 Apr 6;160(2):225–229. doi: 10.1007/BF00267485. [DOI] [PubMed] [Google Scholar]
  5. Freedberg W. B., Lin E. C. Three kinds of controls affecting the expression of the glp regulon in Escherichia coli. J Bacteriol. 1973 Sep;115(3):816–823. doi: 10.1128/jb.115.3.816-823.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Guest J. R. Partial replacement of succinate dehydrogenase function by phage- and plasmid-specified fumarate reductase in Escherichia coli. J Gen Microbiol. 1981 Feb;122(2):171–179. doi: 10.1099/00221287-122-2-171. [DOI] [PubMed] [Google Scholar]
  7. HIRSCH C. A., RASMINSKY M., DAVIS B. D., LIN E. C. A FUMARATE REDUCTASE IN ESCHERICHIA COLI DISTINCT FROM SUCCINATE DEHYDROGENASE. J Biol Chem. 1963 Nov;238:3770–3774. [PubMed] [Google Scholar]
  8. Ingledew W. J., Poole R. K. The respiratory chains of Escherichia coli. Microbiol Rev. 1984 Sep;48(3):222–271. doi: 10.1128/mr.48.3.222-271.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Iuchi S., Kuritzkes D. R., Lin E. C. Escherichia coli mutant with altered respiratory control of the frd operon. J Bacteriol. 1985 Mar;161(3):1023–1028. doi: 10.1128/jb.161.3.1023-1028.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Kay W. W., Kornberg H. L. Genetic control of the uptake of C(4)-dicarboxylic acids by Escherichia coli. FEBS Lett. 1969 Apr;3(2):93–96. doi: 10.1016/0014-5793(69)80105-5. [DOI] [PubMed] [Google Scholar]
  12. Kay W. W., Kornberg H. L. The uptake of C4-dicarboxylic acids by Escherichia coli. Eur J Biochem. 1971 Jan;18(2):274–281. doi: 10.1111/j.1432-1033.1971.tb01240.x. [DOI] [PubMed] [Google Scholar]
  13. Kistler W. S., Hirsch C. A., Cozzarelli N. R., Lin E. C. Second pyridine nucleotide-independent 1-alpha-glycerophosphate dehydrogenase in Escherichia coli K-12. J Bacteriol. 1969 Nov;100(2):1133–1135. doi: 10.1128/jb.100.2.1133-1135.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kistler W. S., Lin E. C. Anaerobic L- -glycerophosphate dehydrogenase of Escherichia coli: its genetic locus and its physiological role. J Bacteriol. 1971 Dec;108(3):1224–1234. doi: 10.1128/jb.108.3.1224-1234.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kistler W. S., Lin E. C. Purification and properties of the flavine-stimulated anaerobic L- -glycerophosphate dehydrogenase of Escherichia coli. J Bacteriol. 1972 Oct;112(1):539–547. doi: 10.1128/jb.112.1.539-547.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Konings W. N., Kaback H. R. Anaerobic transport in Escherichia coli membrane vesicles. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3376–3381. doi: 10.1073/pnas.70.12.3376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kuritzkes D. R., Zhang X. Y., Lin E. C. Use of phi(glp-lac) in studies of respiratory regulation of the Escherichia coli anaerobic sn-glycerol-3-phosphate dehydrogenase genes (glpAB). J Bacteriol. 1984 Feb;157(2):591–598. doi: 10.1128/jb.157.2.591-598.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  19. Lambden P. R., Guest J. R. Mutants of Escherichia coli K12 unable to use fumarate as an anaerobic electron acceptor. J Gen Microbiol. 1976 Dec;97(2):145–160. doi: 10.1099/00221287-97-2-145. [DOI] [PubMed] [Google Scholar]
  20. Lin E. C. Glycerol dissimilation and its regulation in bacteria. Annu Rev Microbiol. 1976;30:535–578. doi: 10.1146/annurev.mi.30.100176.002535. [DOI] [PubMed] [Google Scholar]
  21. Maloy S. R., Roth J. R. Regulation of proline utilization in Salmonella typhimurium: characterization of put::Mu d(Ap, lac) operon fusions. J Bacteriol. 1983 May;154(2):561–568. doi: 10.1128/jb.154.2.561-568.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Miki K., Lin E. C. Anaerobic energy-yielding reaction associated with transhydrogenation from glycerol 3-phosphate to fumarate by an Escherichia coli system. J Bacteriol. 1975 Dec;124(3):1282–1287. doi: 10.1128/jb.124.3.1282-1287.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Newman B. M., Cole J. A. The chromosomal location and pleiotropic effects of mutations of the nirA+ gene of Escherichia coli K12: the essential role of nirA+ in nitrite reduction and in other anaerobic redox reactions. J Gen Microbiol. 1978 May;106(1):1–12. doi: 10.1099/00221287-106-1-1. [DOI] [PubMed] [Google Scholar]
  24. Postma P. W., Lengeler J. W. Phosphoenolpyruvate:carbohydrate phosphotransferase system of bacteria. Microbiol Rev. 1985 Sep;49(3):232–269. doi: 10.1128/mr.49.3.232-269.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ruíz-Herrera J., García L. G. Regulation of succinate dehydrogenase in Escherichia coli. J Gen Microbiol. 1972 Aug;72(1):29–35. doi: 10.1099/00221287-72-1-29. [DOI] [PubMed] [Google Scholar]
  26. Shaw D. J., Guest J. R. Amplification and product identification of the fnr gene of Escherichia coli. J Gen Microbiol. 1982 Oct;128(10):2221–2228. doi: 10.1099/00221287-128-10-2221. [DOI] [PubMed] [Google Scholar]
  27. Shaw D. J., Rice D. W., Guest J. R. Homology between CAP and Fnr, a regulator of anaerobic respiration in Escherichia coli. J Mol Biol. 1983 May 15;166(2):241–247. doi: 10.1016/s0022-2836(83)80011-4. [DOI] [PubMed] [Google Scholar]
  28. Stewart V., MacGregor C. H. Nitrate reductase in Escherichia coli K-12: involvement of chlC, chlE, and chlG loci. J Bacteriol. 1982 Aug;151(2):788–799. doi: 10.1128/jb.151.2.788-799.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tanaka S., Lerner S. A., Lin E. C. Replacement of a phosphoenolpyruvate-dependent phosphotransferase by a nicotinamide adenine dinucleotide-linked dehydrogenase for the utilization of mannitol. J Bacteriol. 1967 Feb;93(2):642–648. doi: 10.1128/jb.93.2.642-648.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wimpenny J. W., Cole J. A. The regulation of metabolism in facultative bacteria. 3. The effect of nitrate. Biochim Biophys Acta. 1967 Oct 9;148(1):233–242. doi: 10.1016/0304-4165(67)90298-x. [DOI] [PubMed] [Google Scholar]
  31. Wood D., Darlison M. G., Wilde R. J., Guest J. R. Nucleotide sequence encoding the flavoprotein and hydrophobic subunits of the succinate dehydrogenase of Escherichia coli. Biochem J. 1984 Sep 1;222(2):519–534. doi: 10.1042/bj2220519. [DOI] [PMC free article] [PubMed] [Google Scholar]

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