Abstract
Escherichia coli varies the synthesis of many of its respiratory enzymes in response to oxygen availability. These enzymes include cytochrome o oxidase (cyoABCDE) and cytochrome d oxidase (cydAB), used during aerobic cell growth, and a fumarate reductase (frdABCD), dimethyl sulfoxide/trimethylamine oxide reductase (dmsABC), and nitrate reductase (narGHJI), used during anaerobic respiratory conditions. To determine how different levels of oxygen affect the expression of each operon, strains containing cyo-lacZ, cyd-lacZ, frdA-lacZ, dmsA-lacZ, and narG-lacZ fusions were grown in continuous culture at various degrees of air saturation. The basal-level expression of the anaerobic respiratory genes, frdABCD, dmsABC, and narGHJI, occurred when the air saturation of the medium was above 20%; as the saturation was reduced to below 10% (ca. 2% oxygen), the expression rapidly increased and reached a maximal level at 0% air. In contrast, cyoABCDE gene expression was lowest under anaerobic conditions while cyd-lacZ expression was about 40% of its maximum level. When the oxygen level was raised into the microaerophilic range (ca. 7% air saturation) cyd-lacZ expression was maximal while cyo-lacZ expression was elevated by about fivefold. As the air level was raised to above 20% saturation, cyd-lacZ expression fell to a basal level while cyo-lacZ expression was increased to its maximum level. The role of the Fnr and ArcA regulatory proteins in this microaerophilic control of respiratory gene expression was documented: whereas Fnr function as an aerobic/anaerobic switch in the range of 0 to 10% air saturation, ArcA exerted its control in the 10 to 20% range. These two transcriptional regulators coordinate the hierarchial control of respiratory pathway gene expression in E. coli to ensure the optimal use of oxygen in the cell environment.
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- 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]
- Cotter P. A., Gunsalus R. P. 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. 1992 Feb 1;70(1):31–36. doi: 10.1016/0378-1097(92)90558-6. [DOI] [PubMed] [Google Scholar]
- 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]
- Fu H. A., Iuchi S., Lin E. C. The requirement of ArcA and Fnr for peak expression of the cyd operon in Escherichia coli under microaerobic conditions. Mol Gen Genet. 1991 Apr;226(1-2):209–213. doi: 10.1007/BF00273605. [DOI] [PubMed] [Google Scholar]
- 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]
- Gunsalus R. P., Park S. J. Aerobic-anaerobic gene regulation in Escherichia coli: control by the ArcAB and Fnr regulons. Res Microbiol. 1994 Jun-Aug;145(5-6):437–450. doi: 10.1016/0923-2508(94)90092-2. [DOI] [PubMed] [Google Scholar]
- Iuchi S., Chepuri V., Fu H. A., Gennis R. B., Lin E. C. 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. 1990 Oct;172(10):6020–6025. doi: 10.1128/jb.172.10.6020-6025.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Iuchi S., Lin E. C. Adaptation of Escherichia coli to respiratory conditions: regulation of gene expression. Cell. 1991 Jul 12;66(1):5–7. doi: 10.1016/0092-8674(91)90130-q. [DOI] [PubMed] [Google Scholar]
- Iuchi S., Lin E. C. Purification and phosphorylation of the Arc regulatory components of Escherichia coli. J Bacteriol. 1992 Sep;174(17):5617–5623. doi: 10.1128/jb.174.17.5617-5623.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Iuchi S. Phosphorylation/dephosphorylation of the receiver module at the conserved aspartate residue controls transphosphorylation activity of histidine kinase in sensor protein ArcB of Escherichia coli. J Biol Chem. 1993 Nov 15;268(32):23972–23980. [PubMed] [Google Scholar]
- 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]
- Melville S. B., Gunsalus R. P. Mutations in fnr that alter anaerobic regulation of electron transport-associated genes in Escherichia coli. J Biol Chem. 1990 Nov 5;265(31):18733–18736. [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Tseng C. P., Hansen A. K., Cotter P., Gunsalus R. P. Effect of cell growth rate on expression of the anaerobic respiratory pathway operons frdABCD, dmsABC, and narGHJI of Escherichia coli. J Bacteriol. 1994 Nov;176(21):6599–6605. doi: 10.1128/jb.176.21.6599-6605.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Unden G., Trageser M. Oxygen regulated gene expression in Escherichia coli: control of anaerobic respiration by the FNR protein. Antonie Van Leeuwenhoek. 1991 Feb;59(2):65–76. doi: 10.1007/BF00445650. [DOI] [PubMed] [Google Scholar]