The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool

Journal of Bacteriology

Volumn 192, Issue 3, 2010, Pages 746-754

  Bekker, Martijn ^a   Alexeeva, Svetlana ^a   Laan, Wouter ^a,c   Sawers, Gary ^b   De Mattos, Joost Teixeira ^a   Hellingwerf, Klaas ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARCB PROTEIN; BETA GALACTOSIDASE; MENAQUINONE; PROTEIN DERIVATIVE; UBIQUINONE; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE ACTIVATION; GENE DELETION; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION STATE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REPORTER GENE;

BACTERIAL OUTER MEMBRANE PROTEINS; BLOTTING, WESTERN; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MODELS, GENETIC; OPERON; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASES; REPRESSOR PROTEINS; UBIQUINONE; VITAMIN K 2;

ARCA; ESCHERICHIA COLI;

EID: 75149177776     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01156-09     Document Type: Article

References (42)

1. Alexeeva, S. 2000. Molecular physiology of responses to oxygen in Escherichia coli. Ph.D. thesis. University of Amsterdam, Amsterdam, The Netherlands.
2. Alexeeva, S., B. de Kort, G. Sawers, K. J. Hellingwerf, and M. J. de Mattos. 2000. Effects of limited aeration and of the ArcAB system on intermediary pyruvate catabolism in Escherichia coli. J. Bacteriol. 182:4934-4940.
3. Alexeeva, S., K. J. Hellingwerf, and M. J. Teixeira de Mattos. 2003. Requirement of ArcA for redox regulation in Escherichia coli under microaerobic but not anaerobic or aerobic conditions. J. Bacteriol. 185:204-209.
4. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K. A. Datsenko, M. Tomita, B. L. Wanner, and H. Mori. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008.
5. Bekker, M., G. Kramer, A. F. Hartog, M. J. Wagner, C. G. de Koster, K. J. Hellingwerf, and M. J. de Mattos. 2007. Changes in the redox state and composition of the quinone pool of Escherichia coli during aerobic batchculture growth. Microbiology 153:1974-1980.
6. Bensadoun, A., and D. Weinstein. 1976. Assay of proteins in the presence of interfering materials. Anal. Biochem. 70:241-250.
7. Butler, C. S., S. A. Fairhurst, S. J. Ferguson, A. J. Thomson, B. C. Berks, D. J. Richardson, and D. J. Lowe. 2002. Mo(V) co-ordination in the periplasmic nitrate reductase from Paracoccus pantotrophus probed by electron nuclear double resonance (ENDOR) spectroscopy. Biochem. J. 363:817-823.
8. a.Casadaban, M. J., and S. N. Cohen. 1979. Lactose genes fused to exogenous promoters in one step using Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc. Natl. Acad. Sci. U. S. A. 76:4530-4533.
9. Cotter, P. A., S. B. Melville, J. A. Albrecht, and R. P. Gunsalus. 1997. Aerobic regulation of cytochrome d oxidase (cydAB) operon expression in Escherichia coli: roles of Fnr and ArcA in repression and activation. Mol. Microbiol. 25:605-615.
10. Drapal, N., and G. Sawers. 1995. Purification of ArcA and analysis of its specific interaction with the pfl promoter-regulatory region. Mol. Microbiol. 16:597-607.
11. Evans, C. G. T., D. Herbert, and D. W. Tempest. 1970. The continuous culture of microorganisms. Construction of a chemostat., vol. 2. Academic Press, London, United Kingdom.
12. Georgellis, D., O. Kwon, and E. C. Lin. 2001. Quinones as the redox signal for the arc two-component system of bacteria. Science 292:2314-2316.
13. Georgellis, D., A. S. Lynch, and E. C. Lin. 1997. In vitro phosphorylation study of the arc two-component signal transduction system of Escherichia coli. J. Bacteriol. 179:5429-5435.
14. Giacomini, A., V. Corich, F. J. Ollero, A. Squartini, and M. P. Nuti. 1992. Experimental conditions may affect reproducibility of the beta-galactosidase assay. FEMS Microbiol. Lett. 79:87-90.
15. Govantes, F., J. A. Albrecht, and R. P. Gunsalus. 2000. Oxygen regulation of the Escherichia coli cytochrome d oxidase (cydAB) operon: roles of multiple promoters and the Fnr-1 and Fnr-2 binding sites. Mol. Microbiol. 37:1456-1469.
16. Grammel, H., and R. Ghosh. 2008. Redox-state dynamics of ubiquinone-10 imply cooperative regulation of photosynthetic membrane expression in Rhodospirillum rubrum. J. Bacteriol. 190:4912-4921.
17. Ingledew, W. J., and R. K. Poole. 1984. The respiratory chains of Escherichia coli. Microbiol. Rev. 48:222-271.
18. Iuchi, S., D. C. Cameron, and E. C. Lin. 1989. A second global regulator gene (arcB) mediating repression of enzymes in aerobic pathways of Escherichia coli. J. Bacteriol. 171:868-873.
19. Iuchi, S., and E. C. Lin. 1993. Adaptation of Escherichia coli to redox environments by gene expression. Mol. Microbiol. 9:9-15.
20. Iuchi, S., and E. C. Lin. 1988. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc. Natl. Acad. Sci. U. S. A. 85:1888-1892.
21. Iuchi, S., Z. Matsuda, T. Fujiwara, and E. C. Lin. 1990. The arcB gene of Escherichia coli encodes a sensor-regulator protein for anaerobic repression of the arc modulon. Mol. Microbiol. 4:715-727.
22. Jeon, Y., Y. S. Lee, J. S. Han, J. B. Kim, and D. S. Hwang. 2001. Multimerization of phosphorylated and non-phosphorylated ArcA is necessary for the response regulator function of the Arc two-component signal transduction system. J. Biol. Chem. 276:40873-40879.
23. Keleti, K. 1990. Kinetics of regulatory enzymes, p. 266-284. In Basic enzyme kinetics. MIR, Moscow, Russia.
24. Kwon, O., D. Georgellis, and E. C. Lin. 2000. Phosphorelay as the sole physiological route of signal transmission by the arc two-component system of Escherichia coli. J. Bacteriol. 182:3858-3862.
25. Liu, X., and P. De Wulf. 2004. Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J. Biol. Chem. 279:12588-12597.
26. Lynch, A. S., and E. C. Lin. 1996. Transcriptional control mediated by the ArcA two-component response regulator protein of Escherichia coli: characterization of DNA binding at target promoters. J. Bacteriol. 178:6238-6249.
27. Malpica, R., B. Franco, C. Rodriguez, O. Kwon, and D. Georgellis. 2004. Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc. Natl. Acad. Sci. U. S. A. 101:13318-13323.
28. Matsubara, M., and T. Mizuno. 2000. The SixA phospho-histidine phosphatase modulates the ArcB phosphorelay signal transduction in Escherichia coli. FEBS Lett. 470:118-124.
29. Matsui, H., T. Kurosaki, M. Tokuda, and O. Hatase. 1983. Modulation of optical density by sulfhydryl reagents in microbiuret method: a modified method for protein determination in the presence of sulfhydryl reagents. Acta Med. Okayama 37:125-129.
30. Matsumoto, J., K. Sakamoto, N. Shinjyo, Y. Kido, N. Yamamoto, K. Yagi, H. Miyoshi, N. Nonaka, K. Katakura, K. Kita, and Y. Oku. 2008. Anaerobic NADH-fumarate reductase system is predominant in the respiratory chain of Echinococcus multilocularis, providing a novel target for the chemotherapy of alveolar echinococcosis. Antimicrob. Agents Chemother. 52:164-170.
31. Miller, J. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Potter, L., H. Angove, D. Richardson, and J. Cole. 2001. Nitrate reduction in the periplasm of gram-negative bacteria. Adv. Microb. Physiol. 45:51-112.
33. Ramanujam, P., S. Fogerty, W. Heiser, and J. Jolly. 1990. Fast gel electrophoresis to analyze DNA-protein interactions. Biotechniques 8:556-563.
34. Richardson, D. J., B. C. Berks, D. A. Russell, S. Spiro, and C. J. Taylor. 2001. Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell. Mol. Life Sci. 58:165-178.
35. Rodriguez, C., O. Kwon, and D. Georgellis. 2004. Effect of D-lactate on the physiological activity of the ArcB sensor kinase in Escherichia coli. J. Bacteriol. 186:2085-2090.
36. Sawers, G. 1993. Specific transcriptional requirements for positive regulation of the anaerobically inducible pfl operon by ArcA and FNR. Mol. Microbiol. 10:737-747.
37. Sawers, G., and B. Suppmann. 1992. Anaerobic induction of pyruvate formate-lyase gene expression is mediated by the ArcA and FNR proteins. J. Bacteriol. 174:3474-3478.
38. Segel, I. 1993. Multisite and allosteric enzymes. John Wiley & Sons, Inc., New York, NY.
39. Shestopalov, A. I., A. V. Bogachev, R. A. Murtazina, M. B. Viryasov, and V. P. Skulachev. 1997. Aeration-dependent changes in composition of the quinone pool in Escherichia coli. Evidence of post-transcriptional regulation of the quinone biosynthesis. FEBS Lett. 404:272-274.
40. Simons, R. W., F. Houman, and N. Kleckner. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53:85-96.
41. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76:4350-4354.
42. Unden, G., and J. Bongaerts. 1997. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim. Biophys. Acta 1320:217-234.