1887

Abstract

ArcA is a global transcription factor required for optimal growth of during anaerobic growth. In this study, the role of ArcA on the transcriptional regulatory subnetwork of the regulon was investigated. Gene expression profiles of deletion mutants (Δ, Δ and Δ) indicated that (i) ArcA is a major transcription factor for the transcriptional regulation of fatty acid metabolism in the absence of oxygen, and (ii) ArcA and FadR cooperatively regulate the regulon under anaerobic conditions. To determine the direct interaction between ArcA and the promoters of the regulon genes, chromatin immunoprecipitation (ChIP) analysis was performed. ChIP analysis suggested that ArcA directly binds to the promoter regions of the regulon genes . An ArcA-binding motif was identified from known binding sequences and predicted putative binding sites in the promoter regions of the regulon genes. These results indicate that ArcA directly represses the expression of regulon genes during anaerobic growth.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28912-0
2006-08-01
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/8/2207.html?itemId=/content/journal/micro/10.1099/mic.0.28912-0&mimeType=html&fmt=ahah

References

  1. Berg, B. V. D., Black, P. N., Clemons, W. M., Jr & Rapoport, T. A. ( 2004; ). Crystal structure of the long-chain fatty acid transporter FadL. Science 304, 1506–1509.[CrossRef]
    [Google Scholar]
  2. Binstock, J. F., Pramanik, A. & Schulz, H. ( 1977; ). Isolation of a multi-enzyme complex of fatty acid oxidation from Escherichia coli. Proc Natl Acad Sci U S A 74, 492–495.[CrossRef]
    [Google Scholar]
  3. Black, P. N. ( 1991; ). Primary sequence of the Escherichia coli fadL gene encoding an outer membrane protein required for long-chain fatty acid transport. J Bacteriol 173, 435–442.
    [Google Scholar]
  4. Black, P. N., DiRusso, C. C., Metzger, A. K. & Heimert, T. L. ( 1992; ). Cloning, sequencing, and expression of the fadD gene of Escherichia coli encoding acyl coenzyme A synthetase. J Biol Chem 267, 25513–25520.
    [Google Scholar]
  5. Bongaerts, J., Zoske, S., Weidner, U. & Unden, G. ( 1995; ). Transcriptional regulation of the proton translocating NADH dehydrogenase genes (nuoA–N) of Escherichia coli by electron acceptors, electron donors and gene regulators. Mol Microbiol 16, 521–534.[CrossRef]
    [Google Scholar]
  6. Busch, W. & Saier, M. H., Jr ( 2002; ). The transporter classification (TC) system. Crit Rev Biochem Mol Biol 37, 287–337.[CrossRef]
    [Google Scholar]
  7. Campbell, J. W. & Cronan, J. E., Jr ( 2002; ). The enigmatic Escherichia coli fadE gene is yafH. J Bacteriol 184, 3759–3764.[CrossRef]
    [Google Scholar]
  8. Campbell, J. W., Morgan-Kiss, R. M. & Cronan, J. E., Jr ( 2003; ). A new Escherichia coli metabolic competency: growth on fatty acids by a novel anaerobic β-oxidation pathway. Mol Microbiol 47, 793–805.[CrossRef]
    [Google Scholar]
  9. Chao, G., Shen, J., Tseng, C. P., Park, S.-J. & Gunsalus, R. P. ( 1997; ). Aerobic regulation of isocitrate dehydrogenase gene (icd) expression in Escherichia coli by the arcA and fnr gene products. J Bacteriol 179, 4299–4304.
    [Google Scholar]
  10. Cho, B.-K., Knight, E. M. & Palsson, B. O. ( 2006; ). PCR-based tandem epitope tagging system for Escherichia coli genome engineering. Biotechniques 40, 67–72.[CrossRef]
    [Google Scholar]
  11. Clark, D. P. & Cronan, J. E., Jr ( 1996; ). Two-carbon compounds and fatty acids as carbon sources. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, pp. 343–357. Edited by F. C. Neidhardt. Washington, DC: American Society for Microbiology.
  12. Covert, M. W., Knight, E. M., Reed, J. L., Herrgard, M. J. & Palsson, B. O. ( 2004; ). Integrating high-throughput and computational data elucidates bacterial network. Nature 429, 92–96.[CrossRef]
    [Google Scholar]
  13. Cronan, J. E., Jr & Subrahmanyam, S. ( 1998; ). FadR, transcriptional co-ordination of metabolic expediency. Mol Microbiol 29, 937–943.[CrossRef]
    [Google Scholar]
  14. Cunningham, L., Gruer, M. J. & Guest, J. R. ( 1997; ). Transcriptional regulation of the aconitase genes (acnA and acnB) of Escherichia coli. Microbiology 143, 3795–3805.[CrossRef]
    [Google Scholar]
  15. Cunningham, L., Georgellis, D., Green, J. & Guest, J. R. ( 1998; ). Co-regulation of lipoamide dehydrogenase and 2-oxoglutarate dehydrogenase synthesis in Escherichia coli: characterisation of an ArcA binding site in the lpd promoter. FEMS Microbiol Lett 169, 403–408.[CrossRef]
    [Google Scholar]
  16. Datsenko, K. A. & Wanner, B. L. ( 2000; ). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640–6645.[CrossRef]
    [Google Scholar]
  17. DiRusso, C. C. & Nystrom, T. ( 1998; ). The fats of Escherichia coli during infancy and old age: regulation by global regulators, alarmones and lipid intermediates. Mol Microbiol 27, 1–8.[CrossRef]
    [Google Scholar]
  18. DiRusso, C. C., Heimert, T. L. & Metzger, A. K. ( 1992; ). Characterization of FadR, a global transcriptional regulator of fatty acid metabolism in Escherichia coli. J Biol Chem 267, 8685–8691.
    [Google Scholar]
  19. Drapal, N. & Sawers, G. ( 1995; ). Purification of ArcA and analysis of its specific interaction with the pfl promoter-regulatory region. Mol Microbiol 16, 597–607.[CrossRef]
    [Google Scholar]
  20. Georgellis, D., Lynch, A. S. & Lin, E. C. C. ( 1997; ). In vitro phosphorylation study of the arc two-component signal transduction system of Escherichia coli. J Bacteriol 179, 5429–5435.
    [Google Scholar]
  21. Georgellis, D., Kwon, O. & Lin, E. C. C. ( 2001; ). Quinones as the redox signal for the arc two-component system of bacteria. Science 292, 2314–2316.[CrossRef]
    [Google Scholar]
  22. Govantes, F., Orjalo, A. V. & Gunsalus, R. P. ( 2000; ). Interplay between three global regulatory proteins mediates oxygen regulation of the Escherichia coli cytochrome d oxidase (cydAB) operon. Mol Microbiol 38, 1061–1073.
    [Google Scholar]
  23. Henry, M. F. & Cronan, J. E., Jr ( 1992; ). A new mechanism of transcriptional regulation: release of an activator triggered by small molecule binding. Cell 70, 671–679.[CrossRef]
    [Google Scholar]
  24. Higashitani, A. Y., Nishimura, Y., Hara, H., Aiba, H., Mizuno, T. & Horiuchi, K. ( 1993; ). Osmoregulation of the fatty acid receptor gene fadL in Escherichia coli. Mol Gen Genet 240, 339–347.
    [Google Scholar]
  25. Ishige, K., Nagasawa, S., Tokishita, S. & Mizuno, T. ( 1994; ). A novel device of bacterial signal transducers. EMBO J 13, 5195–5202.
    [Google Scholar]
  26. Iuchi, S. & Lin, E. C. C. ( 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.[CrossRef]
    [Google Scholar]
  27. Iuchi, S. & Lin, E. C. C. ( 1991; ). Adaptation of Escherichia coli to respiratory conditions: regulation of gene expression. Cell 66, 5–7.[CrossRef]
    [Google Scholar]
  28. Iuchi, S. & Lin, E. C. C. ( 1992; ). Purification and phosphorylation of the Arc regulatory components of Escherichia coli. J Bacteriol 174, 5617–5623.
    [Google Scholar]
  29. Jensen, K. F. ( 1993; ). The Escherichia coli K-12 ‘wild types' W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J Bacteriol 175, 3401–3407.
    [Google Scholar]
  30. Jeong, J.-Y., Kim, Y.-J., Cho, N., Shin, D., Nam, T.-W., Ryu, S. & Seok, Y.-J. ( 2004; ). Expression of ptsG encoding the major glucose transporter is regulated by ArcA in Escherichia coli. J Biol Chem 279, 38513–38518.[CrossRef]
    [Google Scholar]
  31. Lamark, T., Rokenes, T. P., McDougall, J. & Strom, A. R. ( 1996; ). The complex bet promoters of Escherichia coli: regulation by oxygen (ArcA), choline (BetI), and osmotic stress. J Bacteriol 178, 1655–1662.
    [Google Scholar]
  32. Lin, E. C. C. & Iuchi, S. ( 1991; ). Regulation of gene expression in fermentative and respiratory systems in Escherichia coli and related bacteria. Annu Rev Genet 25, 361–368.[CrossRef]
    [Google Scholar]
  33. Liu, X. & De Wulf, P. ( 2004; ). Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J Biol Chem 279, 12588–12597.[CrossRef]
    [Google Scholar]
  34. Lockwood, C. R. & Frayling, T. M. ( 2003; ). Combining genome and mouse knockout expression data to highlight binding sites for the transcription factor HNF1α. In silico Biol 3, 57–70.
    [Google Scholar]
  35. Lynch, A. S. & Lin, E. C. C. ( 1996a; ). 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.
    [Google Scholar]
  36. Lynch, A. S. & Lin, E. C. C. ( 1996b; ). Responses to molecular oxygen. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, pp. 1526–1538. Edited by F. C. Neidhardt. Washington, DC: American Society for Microbiology.
  37. Magnuson, K., Jackowski, S., Rock, C. O. & Cronan, J. E., Jr ( 1993; ). Regulation of fatty acid biosynthesis in Escherichia coli. Microbiol Rev 57, 522–542.
    [Google Scholar]
  38. Malpica, R., Franco, B., Rodriguez, C., Kwon, O. & Georgellis, D. ( 2004; ). Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc Natl Acad Sci U S A 101, 13318–13323.[CrossRef]
    [Google Scholar]
  39. McGuire, A. M., De Wulf, P., Church, G. M. & Lin, E. C. C. ( 1999; ). A weight matrix for binding recognition by the redox-response regulator ArcA-P of Escherichia coli. Mol Microbiol 32, 219–221.[CrossRef]
    [Google Scholar]
  40. Morgan-Kiss, R. M. & Cronan, J. E., Jr ( 2004; ). The Escherichia coli fadK (ydiD) gene encodes an anaerobically regulated short chain acyl-CoA synthetase. J Biol Chem 279, 37324–37333.[CrossRef]
    [Google Scholar]
  41. Nunn, W. D. ( 1986; ). A molecular view of fatty acid catabolism in Escherichia coli. Microbiol Rev 50, 179–192.
    [Google Scholar]
  42. Park, S.-J., Cotter, P. A. & Gunsalus, R. P. ( 1995; ). Regulation of malate dehydrogenase (mdh) gene expression in Escherichia coli in response to oxygen, carbon and heme availability. J Bacteriol 177, 6652–6656.
    [Google Scholar]
  43. Pauli, G., Ehring, R. & Overath, P. ( 1974; ). Fatty acid degradation in Escherichia coli: requirement of cyclic adenosine monophosphate and cyclic adenosine monophosphate receptor protein for enzyme synthesis. J Bacteriol 117, 1178–1183.
    [Google Scholar]
  44. Pellicer, M. T., Lynch, A. S., De Wulf, P., Boyd, D., Aguilar, J. & Lin, E. C. C. ( 1999a; ). A mutational study of the ArcA-P binding sequences in the aldA promoter of Escherichia coli. Mol Gen Genet 261, 170–176.[CrossRef]
    [Google Scholar]
  45. Pellicer, M. T., Fernandez, C., Badia, J., Aguilar, J., Lin, E. C. C. & Baldoma, L. ( 1999b; ). Cross-induction of glc and ace operons of Escherichia coli attributable to pathway intersection: characterization of the glc promoter. J Biol Chem 274, 1745–1752.[CrossRef]
    [Google Scholar]
  46. Pramanik, A., Pawar, S., Antonian, E. & Schulz, H. ( 1979; ). Five different enzymatic activities are associated with the multienzyme complex of fatty acid oxidation from Escherichia coli. J Bacteriol 137, 469–473.
    [Google Scholar]
  47. Robison, K., McGuire, A. M. & Church, G. M. ( 1998; ). A comprehensive library of DNA-binding site matrices for 55 proteins applied to the complete Escherichia coli K-12 genome. J Mol Biol 284, 241–254.[CrossRef]
    [Google Scholar]
  48. Sallus, L., Haselbeck, R. J. & Nunn, W. D. ( 1983; ). Regulation of fatty acid transport in Escherichia coli: analysis by operon fusion. J Bacteriol 155, 1450–1454.
    [Google Scholar]
  49. Schulz, H. ( 1991; ). Beta oxidation of fatty acids. Biochim Biophys Acta 1081, 109–120.[CrossRef]
    [Google Scholar]
  50. Shen, J. & Gunsalus, R. P. ( 1997; ). Role of multiple ArcA recognition sites in anaerobic regulation of succinate dehydrogenase (sdhCDAB) gene expression in Escherichia coli. Mol Microbiol 26, 223–236.[CrossRef]
    [Google Scholar]
  51. Strohmaier, H., Noiges, R., Kotschan, S., Sawers, G., Hogenauer, G., Zechner, E. L. & Koraimann, G. ( 1998; ). Signal transduction and bacterial conjugation: characterization of the role of ArcA in regulating conjugative transfer of the resistance plasmid R1. J Mol Biol 277, 309–316.[CrossRef]
    [Google Scholar]
  52. Tardat, B. & Touati, D. ( 1993; ). Iron and oxygen regulation of Escherichia coli MnSOD expression: competition between the global regulators Fur and ArcA for binding to DNA. Mol Microbiol 9, 53–63.[CrossRef]
    [Google Scholar]
  53. Tsuzuki, M., Ishige, K. & Mizuno, T. ( 1995; ). Phosphotransfer circuitry of the putative multi-signal transducer, ArcB, of Escherichia coli: in vitro studies with mutants. Mol Microbiol 18, 953–962.[CrossRef]
    [Google Scholar]
  54. Xu, Y., Heath, R. J., Li, Z., Rock, C. O. & White, S. W. ( 2001; ). The FadR.DNA complex. J Biol Chem 276, 17373–17379.[CrossRef]
    [Google Scholar]
  55. Yamamoto, K., Hirao, K., Oshima, T., Aiba, H., Utsumi, R. & Ishihama, A. ( 2005; ). Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 280, 1448–1456.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28912-0
Loading
/content/journal/micro/10.1099/mic.0.28912-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error