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. 1990 Oct;172(10):6020–6025. doi: 10.1128/jb.172.10.6020-6025.1990

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.

S Iuchi 1, V Chepuri 1, H A Fu 1, R B Gennis 1, E C Lin 1
PMCID: PMC526924  PMID: 2170337

Abstract

Escherichia coli has two terminal oxidases for its respiratory chain: cytochrome o (low O2 affinity) and cytochrome d (high O2 affinity). Expression of the cyo operon, encoding cytochrome o, is decreased by anaerobic growth, whereas expression of the cyd operon, encoding cytochrome d, is increased by anaerobic growth. We show by the use of lac gene fusion that the expressions of cyo and cyd are under the control of the two-component arc system. In a cyo+ cyd+ background, expression of phi(cyo-lac) is higher when the organism is grown aerobically than when it is grown anaerobically. A mutation in either the sensor gene arcB or the pleiotropic regulator gene arcA almost abolishes the anaerobic repression. In the same background, expression of phi(cyd-lac) is higher under anaerobic growth conditions than under aerobic growth conditions. A mutation in arcA or arcB lowers both the aerobic and anaerobic expressions, suggesting that ArcA plays an activating role instead of the typical repressing role. Under aerobic growth conditions, double deletions of cyo and cyd lower phi(cyo-lac) expression but enhance phi(cyd-lac) expression. The double deletions also prevent elevated aerobic induction of the lct operon (encoding L-lactate dehydrogenase), another target operon of the arc system. In contrast, these deletions do not circumvent aerobic repression of the nar operon (encoding the anaerobic respiratory enzyme nitrate reductase) under the control of the pleiotropic fnr gene product. It thus appears that ArcB senses the presence of O2 by level of an electron transport component in reduced form or that of an nonautoxidizable compound linked to the process by a redox reaction, whereas Fnr senses O2 by a different mechanism.

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Selected References

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  1. Au D. C., Gennis R. B. Cloning of the cyo locus encoding the cytochrome o terminal oxidase complex of Escherichia coli. J Bacteriol. 1987 Jul;169(7):3237–3242. doi: 10.1128/jb.169.7.3237-3242.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Drury L. S., Buxton R. S. DNA sequence analysis of the dye gene of Escherichia coli reveals amino acid homology between the dye and OmpR proteins. J Biol Chem. 1985 Apr 10;260(7):4236–4242. [PubMed] [Google Scholar]
  4. Georgiou C. D., Dueweke T. J., Gennis R. B. Regulation of expression of the cytochrome d terminal oxidase in Escherichia coli is transcriptional. J Bacteriol. 1988 Feb;170(2):961–966. doi: 10.1128/jb.170.2.961-966.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Green G. N., Gennis R. B. Isolation and characterization of an Escherichia coli mutant lacking cytochrome d terminal oxidase. J Bacteriol. 1983 Jun;154(3):1269–1275. doi: 10.1128/jb.154.3.1269-1275.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hattori M., Sakaki Y. Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986 Feb 1;152(2):232–238. doi: 10.1016/0003-2697(86)90403-3. [DOI] [PubMed] [Google Scholar]
  7. Iuchi S., Cameron D. C., Lin E. C. A second global regulator gene (arcB) mediating repression of enzymes in aerobic pathways of Escherichia coli. J Bacteriol. 1989 Feb;171(2):868–873. doi: 10.1128/jb.171.2.868-873.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Iuchi S., Lin E. C. Molybdenum effector of fumarate reductase repression and nitrate reductase induction in Escherichia coli. J Bacteriol. 1987 Aug;169(8):3720–3725. doi: 10.1128/jb.169.8.3720-3725.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Iuchi S., Lin E. C. The narL gene product activates the nitrate reductase operon and represses the fumarate reductase and trimethylamine N-oxide reductase operons in Escherichia coli. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3901–3905. doi: 10.1073/pnas.84.11.3901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Iuchi S., Lin E. C. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1888–1892. doi: 10.1073/pnas.85.6.1888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Iuchi S., Matsuda Z., Fujiwara T., Lin E. C. The arcB gene of Escherichia coli encodes a sensor-regulator protein for anaerobic repression of the arc modulon. Mol Microbiol. 1990 May;4(5):715–727. doi: 10.1111/j.1365-2958.1990.tb00642.x. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Kita K., Konishi K., Anraku Y. Terminal oxidases of Escherichia coli aerobic respiratory chain. II. Purification and properties of cytochrome b558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems. J Biol Chem. 1984 Mar 10;259(5):3375–3381. [PubMed] [Google Scholar]
  14. Kranz R. G., Gennis R. B. Immunological characterization of the cytochrome o terminal oxidase from Escherichia coli. J Biol Chem. 1983 Sep 10;258(17):10614–10621. [PubMed] [Google Scholar]
  15. 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]
  16. Manoil C., Beckwith J. TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8129–8133. doi: 10.1073/pnas.82.23.8129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Minagawa J., Nakamura H., Yamato I., Mogi T., Anraku Y. Transcriptional regulation of the cytochrome b562-o complex in Escherichia coli. Gene expression and molecular characterization of the promoter. J Biol Chem. 1990 Jul 5;265(19):11198–11203. [PubMed] [Google Scholar]
  18. 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]
  19. Nixon B. T., Ronson C. W., Ausubel F. M. Two-component regulatory systems responsive to environmental stimuli share strongly conserved domains with the nitrogen assimilation regulatory genes ntrB and ntrC. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7850–7854. doi: 10.1073/pnas.83.20.7850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ostrow K. S., Silhavy T. J., Garrett S. cis-acting sites required for osmoregulation of ompF expression in Escherichia coli K-12. J Bacteriol. 1986 Dec;168(3):1165–1171. doi: 10.1128/jb.168.3.1165-1171.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pabo C. O., Sauer R. T. Protein-DNA recognition. Annu Rev Biochem. 1984;53:293–321. doi: 10.1146/annurev.bi.53.070184.001453. [DOI] [PubMed] [Google Scholar]
  22. Pudek M. R., Bragg P. D. Inhibition by cyanide of the respiratory chain oxidases of Escherichia coli. Arch Biochem Biophys. 1974 Oct;164(2):682–693. doi: 10.1016/0003-9861(74)90081-2. [DOI] [PubMed] [Google Scholar]
  23. Rice C. W., Hempfling W. P. Oxygen-limited continuous culture and respiratory energy conservation in Escherichia coli. J Bacteriol. 1978 Apr;134(1):115–124. doi: 10.1128/jb.134.1.115-124.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ronson C. W., Nixon B. T., Ausubel F. M. Conserved domains in bacterial regulatory proteins that respond to environmental stimuli. Cell. 1987 Jun 5;49(5):579–581. doi: 10.1016/0092-8674(87)90530-7. [DOI] [PubMed] [Google Scholar]
  25. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Spiro S., Roberts R. E., Guest J. R. FNR-dependent repression of the ndh gene of Escherichia coli and metal ion requirement for FNR-regulated gene expression. Mol Microbiol. 1989 May;3(5):601–608. doi: 10.1111/j.1365-2958.1989.tb00207.x. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Trageser M., Unden G. Role of cysteine residues and of metal ions in the regulatory functioning of FNR, the transcriptional regulator of anaerobic respiration in Escherichia coli. Mol Microbiol. 1989 May;3(5):593–599. doi: 10.1111/j.1365-2958.1989.tb00206.x. [DOI] [PubMed] [Google Scholar]
  30. Unden G., Trageser M., Duchêne A. Effect of positive redox potentials (greater than +400 mV) on the expression of anaerobic respiratory enzymes in Escherichia coli. Mol Microbiol. 1990 Feb;4(2):315–319. doi: 10.1111/j.1365-2958.1990.tb00598.x. [DOI] [PubMed] [Google Scholar]

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