Abstract
The expression of the cydDC operon was investigated by using a chromosomal phi(cydD-lacZ) transcriptional fusion and primer extension analysis. A single transcriptional start site was found for cydD located 68 bp upstream of the translational start site, and Northern blot analysis confirmed that cydDC is transcribed as a polycistronic message independently of the upstream gene trxB. cydDC was highly expressed under aerobic growth conditions and during anaerobic growth with alternative electron acceptors. Aerobic expression was independent of ArcA and Fnr, but induction of cydDC by nitrate and nitrite was dependent on NarL and Fnr.
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- Aguilar G. R., Soberón M. Cloning and sequence analysis of the Rhizobium etli ccmA and ccmB genes involved in c-type cytochrome biogenesis. Gene. 1996 Dec 5;182(1-2):129–135. doi: 10.1016/s0378-1119(96)00534-3. [DOI] [PubMed] [Google Scholar]
- Altuvia S., Almirón M., Huisman G., Kolter R., Storz G. The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol Microbiol. 1994 Jul;13(2):265–272. doi: 10.1111/j.1365-2958.1994.tb00421.x. [DOI] [PubMed] [Google Scholar]
- Avetisyan A. V., Dibrov P. A., Semeykina A. L., Skulachev V. P., Sokolov M. V. Adaptation of Bacillus FTU and Escherichia coli to alkaline conditions: the Na(+)-motive respiration. Biochim Biophys Acta. 1991 Dec 3;1098(1):95–104. [PubMed] [Google Scholar]
- Bebbington K. J., Williams H. D. Investigation of the role of the cydD gene product in production of a functional cytochrome d oxidase in Escherichia coli. FEMS Microbiol Lett. 1993 Aug 15;112(1):19–24. doi: 10.1111/j.1574-6968.1993.tb06417.x. [DOI] [PubMed] [Google Scholar]
- Beckman D. L., Trawick D. R., Kranz R. G. Bacterial cytochromes c biogenesis. Genes Dev. 1992 Feb;6(2):268–283. doi: 10.1101/gad.6.2.268. [DOI] [PubMed] [Google Scholar]
- Bogachev A. V., Murtazine R. A., Shestopalov A. I., Skulachev V. P. Induction of the Escherichia coli cytochrome d by low delta mu H+ and by sodium ions. Eur J Biochem. 1995 Aug 15;232(1):304–308. doi: 10.1111/j.1432-1033.1995.tb20812.x. [DOI] [PubMed] [Google Scholar]
- Chung C. T., Niemela S. L., Miller R. H. One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2172–2175. doi: 10.1073/pnas.86.7.2172. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collado-Vides J., Magasanik B., Gralla J. D. Control site location and transcriptional regulation in Escherichia coli. Microbiol Rev. 1991 Sep;55(3):371–394. doi: 10.1128/mr.55.3.371-394.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- D'Mello R., Hill S., Poole R. K. The oxygen affinity of cytochrome bo' in Escherichia coli determined by the deoxygenation of oxyleghemoglobin and oxymyoglobin: Km values for oxygen are in the submicromolar range. J Bacteriol. 1995 Feb;177(3):867–870. doi: 10.1128/jb.177.3.867-870.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Darwin A. J., Li J., Stewart V. Analysis of nitrate regulatory protein NarL-binding sites in the fdnG and narG operon control regions of Escherichia coli K-12. Mol Microbiol. 1996 May;20(3):621–632. doi: 10.1046/j.1365-2958.1996.5491074.x. [DOI] [PubMed] [Google Scholar]
- Delaney J. M., Wall D., Georgopoulos C. Molecular characterization of the Escherichia coli htrD gene: cloning, sequence, regulation, and involvement with cytochrome d oxidase. J Bacteriol. 1993 Jan;175(1):166–175. doi: 10.1128/jb.175.1.166-175.1993. [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]
- Gaballa A., Koedam N., Cornelis P. A cytochrome c biogenesis gene involved in pyoverdine production in Pseudomonas fluorescens ATCC 17400. Mol Microbiol. 1996 Aug;21(4):777–785. doi: 10.1046/j.1365-2958.1996.391399.x. [DOI] [PubMed] [Google Scholar]
- Georgiou C. D., Fang H., Gennis R. B. Identification of the cydC locus required for expression of the functional form of the cytochrome d terminal oxidase complex in Escherichia coli. J Bacteriol. 1987 May;169(5):2107–2112. doi: 10.1128/jb.169.5.2107-2112.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gil A., Kroll R. G., Poole R. K. The cytochrome composition of the meat spoilage bacterium Brochothrix thermosphacta: identification of cytochrome a3-and d-type terminal oxidases under various conditions. Arch Microbiol. 1992;158(3):226–233. doi: 10.1007/BF00290819. [DOI] [PubMed] [Google Scholar]
- Goldman B. S., Gabbert K. K., Kranz R. G. 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. 1996 Nov;178(21):6348–6351. doi: 10.1128/jb.178.21.6348-6351.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldman B. S., Gabbert K. K., Kranz R. G. Use of heme reporters for studies of cytochrome biosynthesis and heme transport. J Bacteriol. 1996 Nov;178(21):6338–6347. doi: 10.1128/jb.178.21.6338-6347.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grove J., Tanapongpipat S., Thomas G., Griffiths L., Crooke H., Cole J. Escherichia coli K-12 genes essential for the synthesis of c-type cytochromes and a third nitrate reductase located in the periplasm. Mol Microbiol. 1996 Feb;19(3):467–481. doi: 10.1046/j.1365-2958.1996.383914.x. [DOI] [PubMed] [Google Scholar]
- Guest J. R. Oxygen-regulated gene expression in Escherichia coli. The 1992 Marjory Stephenson Prize Lecture. J Gen Microbiol. 1992 Nov;138(11):2253–2263. doi: 10.1099/00221287-138-11-2253. [DOI] [PubMed] [Google Scholar]
- Higgins C. F. ABC transporters: from microorganisms to man. Annu Rev Cell Biol. 1992;8:67–113. doi: 10.1146/annurev.cb.08.110192.000435. [DOI] [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]
- Kawamukai M., Utsumi R., Takeda K., Higashi A., Matsuda H., Choi Y. L., Komano T. Nucleotide sequence and characterization of the sfs1 gene: sfs1 is involved in CRP*-dependent mal gene expression in Escherichia coli. J Bacteriol. 1991 Apr;173(8):2644–2648. doi: 10.1128/jb.173.8.2644-2648.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lazar S. W., Kolter R. SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol. 1996 Mar;178(6):1770–1773. doi: 10.1128/jb.178.6.1770-1773.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Page M. D., Pearce D. A., Norris H. A., Ferguson S. J. The Paracoccus denitrificans ccmA, B and C genes: cloning and sequencing, and analysis of the potential of their products to form a haem or apo- c-type cytochrome transporter. Microbiology. 1997 Feb;143(Pt 2):563–576. doi: 10.1099/00221287-143-2-563. [DOI] [PubMed] [Google Scholar]
- Poole R. K., Anjum M. F., Membrillo-Hernández J., Kim S. O., Hughes M. N., Stewart V. Nitric oxide, nitrite, and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12. J Bacteriol. 1996 Sep;178(18):5487–5492. doi: 10.1128/jb.178.18.5487-5492.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poole R. K., Gibson F., Wu G. The cydD gene product, component of a heterodimeric ABC transporter, is required for assembly of periplasmic cytochrome c and of cytochrome bd in Escherichia coli. FEMS Microbiol Lett. 1994 Apr 1;117(2):217–223. doi: 10.1111/j.1574-6968.1994.tb06768.x. [DOI] [PubMed] [Google Scholar]
- Poole R. K., Hatch L., Cleeter M. W., Gibson F., Cox G. B., Wu G. Cytochrome bd biosynthesis in Escherichia coli: the sequences of the cydC and cydD genes suggest that they encode the components of an ABC membrane transporter. Mol Microbiol. 1993 Oct;10(2):421–430. [PubMed] [Google Scholar]
- Poole R. K., Williams H. D., Downie J. A., Gibson F. Mutations affecting the cytochrome d-containing oxidase complex of Escherichia coli K12: identification and mapping of a fourth locus, cydD. J Gen Microbiol. 1989 Jul;135(7):1865–1874. doi: 10.1099/00221287-135-7-1865. [DOI] [PubMed] [Google Scholar]
- Rabin R. S., Stewart V. Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. J Bacteriol. 1993 Jun;175(11):3259–3268. doi: 10.1128/jb.175.11.3259-3268.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Russel M., Model P. Sequence of thioredoxin reductase from Escherichia coli. Relationship to other flavoprotein disulfide oxidoreductases. J Biol Chem. 1988 Jun 25;263(18):9015–9019. [PubMed] [Google Scholar]
- Siegele D. A., Imlay K. R., Imlay J. A. The stationary-phase-exit defect of cydC (surB) mutants is due to the lack of a functional terminal cytochrome oxidase. J Bacteriol. 1996 Nov;178(21):6091–6096. doi: 10.1128/jb.178.21.6091-6096.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siegele D. A., Kolter R. Isolation and characterization of an Escherichia coli mutant defective in resuming growth after starvation. Genes Dev. 1993 Dec;7(12B):2629–2640. doi: 10.1101/gad.7.12b.2629. [DOI] [PubMed] [Google Scholar]
- Simons R. W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. doi: 10.1016/0378-1119(87)90095-3. [DOI] [PubMed] [Google Scholar]
- Stewart V., Parales J., Jr Identification and expression of genes narL and narX of the nar (nitrate reductase) locus in Escherichia coli K-12. J Bacteriol. 1988 Apr;170(4):1589–1597. doi: 10.1128/jb.170.4.1589-1597.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Stewart V., Yanofsky C. Role of leader peptide synthesis in tryptophanase operon expression in Escherichia coli K-12. J Bacteriol. 1986 Jul;167(1):383–386. doi: 10.1128/jb.167.1.383-386.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Touati D., Jacques M., Tardat B., Bouchard L., Despied S. Lethal oxidative damage and mutagenesis are generated by iron in delta fur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol. 1995 May;177(9):2305–2314. doi: 10.1128/jb.177.9.2305-2314.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tseng C. P., Albrecht J., Gunsalus R. P. Effect of microaerophilic cell growth conditions on expression of the aerobic (cyoABCDE and cydAB) and anaerobic (narGHJI, frdABCD, and dmsABC) respiratory pathway genes in Escherichia coli. J Bacteriol. 1996 Feb;178(4):1094–1098. doi: 10.1128/jb.178.4.1094-1098.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]