1887

Abstract

The BasS–BasR two-component system is known as an iron- and zinc-sensing transcription regulator in , but so far only a few genes have been identified to be under the direct control of phosphorylated BasR. Using Genomic SELEX (systematic evolution of ligands by exponential enrichment) screening, we have identified a total of at least 38 binding sites of phosphorylated BasR on the genome, and based on the BasR-binding sites, have predicted more than 20 novel targets of regulation. By DNase I footprint analysis for high-affinity BasR-binding sites, a direct repeat of a TTAAnnTT sequence was identified as the BasR box. Transcription regulation of the target genes was confirmed after Northern blot analysis of target gene mRNAs from both wild-type and an otherwise isogenic deletion mutant. The BasR regulon can be classified into three groups of genes: group 1 includes the genes for the formation and modification of membrane structure; group 2 includes genes for modulation of membrane functions; and group 3 includes genes for stress-response cell functions, including , the master regulator of biofilm formation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.057745-0
2012-06-01
2019-10-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/6/1482.html?itemId=/content/journal/micro/10.1099/mic.0.057745-0&mimeType=html&fmt=ahah

References

  1. Aiba H. , Adhya S. , de Crombrugghe B. . ( 1981; ). Evidence for two functional gal promoters in intact Escherichia coli cells. . J Biol Chem 256:, 11905–11910.[PubMed]
    [Google Scholar]
  2. Asha H. , Gowrishankar J. . ( 1993; ). Regulation of kdp operon expression in Escherichia coli: evidence against turgor as signal for transcriptional control. . J Bacteriol 175:, 4528–4537.[PubMed]
    [Google Scholar]
  3. Baba T. , Ara T. , Hasegawa M. , Takai Y. , Okumura Y. , Baba M. , Datsenko K. A. , Tomita M. , Wanner B. L. , Mori H. . ( 2006; ). Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. . Mol Syst Biol 2:, 2006, 0008. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bader M. W. , Sanowar S. , Daley M. E. , Schneider A. R. , Cho U. , Xu W. , Klevit R. E. , Le Moual H. , Miller S. I. . ( 2005; ). Recognition of antimicrobial peptides by a bacterial sensor kinase. . Cell 122:, 461–472. [CrossRef] [PubMed]
    [Google Scholar]
  5. Bourret R. B. . ( 2010; ). Receiver domain structure and function in response regulator proteins. . Curr Opin Microbiol 13:, 142–149. [CrossRef] [PubMed]
    [Google Scholar]
  6. Chamnongpol S. , Dodson W. , Cromie M. J. , Harris Z. L. , Groisman E. A. . ( 2002; ). Fe(III)-mediated cellular toxicity. . Mol Microbiol 45:, 711–719. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cotter P. A. , Chepuri V. , Gennis R. B. , Gunsalus R. P. . ( 1990; ). Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. . J Bacteriol 172:, 6333–6338.[PubMed]
    [Google Scholar]
  8. 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] [PubMed]
    [Google Scholar]
  9. Egger L. A. , Park H. , Inouye M. . ( 1997; ). Signal transduction via the histidyl-aspartyl phosphorelay. . Genes Cells 2:, 167–184. [CrossRef] [PubMed]
    [Google Scholar]
  10. Froelich J. M. , Tran K. , Wall D. . ( 2006; ). A pmrA constitutive mutant sensitizes Escherichia coli to deoxycholic acid. . J Bacteriol 188:, 1180–1183. [CrossRef] [PubMed]
    [Google Scholar]
  11. Gao R. , Stock A. M. . ( 2010; ). Molecular strategies for phosphorylation-mediated regulation of response regulator activity. . Curr Opin Microbiol 13:, 160–167. [CrossRef] [PubMed]
    [Google Scholar]
  12. Green G. N. , Kranz R. G. , Lorence R. M. , Gennis R. B. . ( 1984; ). Identification of subunit I as the cytochrome b 558 component of the cytochrome d terminal oxidase complex of Escherichia coli . . J Biol Chem 259:, 7994–7997.[PubMed]
    [Google Scholar]
  13. Groisman E. A. . ( 2001; ). The pleiotropic two-component regulatory system PhoP-PhoQ. . J Bacteriol 183:, 1835–1842. [CrossRef] [PubMed]
    [Google Scholar]
  14. Hagiwara D. , Yamashino T. , Mizuno T. . ( 2004; ). A genome-wide view of the Escherichia coli BasS–BasR two-component system implicated in iron-responses. . Biosci Biotechnol Biochem 68:, 1758–1767. [CrossRef] [PubMed]
    [Google Scholar]
  15. Hantke K. . ( 2001; ). Iron and metal regulation in bacteria. . Curr Opin Microbiol 4:, 172–177. [CrossRef] [PubMed]
    [Google Scholar]
  16. Herrera C. M. , Hankins J. V. , Trent M. S. . ( 2010; ). Activation of PmrA inhibits LpxT-dependent phosphorylation of lipid A promoting resistance to antimicrobial peptides. . Mol Microbiol 76:, 1444–1460. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hoch J. A. . ( 2000; ). Two-component and phosphorelay signal transduction. . Curr Opin Microbiol 3:, 165–170. [CrossRef] [PubMed]
    [Google Scholar]
  18. Ishihama A. . ( 2009; ). The Nucleoid: an Overview. EcoSal – Escherichia coli and Salmonella: Cellular and Molecular Biology. Edited by Boek A. , Curtiss R. III , Kaper J. B. , Karp P. D. , Neidhardt F. C. , Nystrom T. , Slauch J. M. , Squires C. L. , Ussery D. . . Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  19. Ishihama A. . ( 2010; ). Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. . FEMS Microbiol Rev 34:, 628–645.[PubMed]
    [Google Scholar]
  20. Kato A. , Tanabe H. , Utsumi R. . ( 1999; ). Molecular characterization of the PhoP-PhoQ two-component system in Escherichia coli K-12: identification of extracellular Mg2+-responsive promoters. . J Bacteriol 181:, 5516–5520.[PubMed]
    [Google Scholar]
  21. Lee L. J. , Barrett J. A. , Poole R. K. . ( 2005; ). Genome-wide transcriptional response of chemostat-cultured Escherichia coli to zinc. . J Bacteriol 187:, 1124–1134. [CrossRef] [PubMed]
    [Google Scholar]
  22. Menon N. K. , Robbins J. , Wendt J. C. , Shanmugam K. T. , Przybyla A. E. . ( 1991; ). Mutational analysis and characterization of the Escherichia coli hya operon, which encodes [NiFe] hydrogenase 1. . J Bacteriol 173:, 4851–4861.[PubMed]
    [Google Scholar]
  23. Miller S. I. , Ernst R. K. , Bader M. W. . ( 2005; ). LPS, TLR4 and infectious disease diversity. . Nat Rev Microbiol 3:, 36–46. [CrossRef] [PubMed]
    [Google Scholar]
  24. Mizuno T. . ( 1998; ). His-Asp phosphotransfer signal transduction. . J Biochem 123:, 555–563.[PubMed] [CrossRef]
    [Google Scholar]
  25. Nagasawa S. , Ishige K. , Mizuno T. . ( 1993; ). Novel members of the two-component signal transduction genes in Escherichia coli . . J Biochem 114:, 350–357.[PubMed]
    [Google Scholar]
  26. Nies D. H. . ( 2003; ). Efflux-mediated heavy metal resistance in prokaryotes. . FEMS Microbiol Rev 27:, 313–339. [CrossRef] [PubMed]
    [Google Scholar]
  27. Ninfa A. J. , Magasanik B. . ( 1986; ). Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli . . Proc Natl Acad Sci U S A 83:, 5909–5913. [CrossRef] [PubMed]
    [Google Scholar]
  28. Nummila K. , Kilpeläinen I. , Zähringer U. , Vaara M. , Helander I. M. . ( 1995; ). Lipopolysaccharides of polymyxin B-resistant mutants of Escherichia coli are extensively substituted by 2-aminoethyl pyrophosphate and contain aminoarabinose in lipid A. . Mol Microbiol 16:, 271–278. [CrossRef] [PubMed]
    [Google Scholar]
  29. Ogasawara H. , Hasegawa A. , Kanda E. , Miki T. , Yamamoto K. , Ishihama A. . ( 2007a; ). Genomic SELEX search for target promoters under the control of the PhoQP-RstBA signal relay cascade. . J Bacteriol 189:, 4791–4799. [CrossRef] [PubMed]
    [Google Scholar]
  30. Ogasawara H. , Ishida Y. , Yamada K. , Yamamoto K. , Ishihama A. . ( 2007b; ). PdhR (pyruvate dehydrogenase complex regulator) controls the respiratory electron transport system in Escherichia coli . . J Bacteriol 189:, 5534–5541. [CrossRef] [PubMed]
    [Google Scholar]
  31. Ogasawara H. , Yamada K. , Kori A. , Yamamoto K. , Ishihama A. . ( 2010a; ). Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors. . Microbiology 156:, 2470–2483. [CrossRef] [PubMed]
    [Google Scholar]
  32. Ogasawara H. , Yamamoto K. , Ishihama A. . ( 2010b; ). Regulatory role of MlrA in transcription activation of csgD, the master regulator of biofilm formation in Escherichia coli . . FEMS Microbiol Lett 312:, 160–168. [CrossRef] [PubMed]
    [Google Scholar]
  33. Ogasawara H. , Yamamoto K. , Ishihama A. . ( 2011; ). Role of the biofilm master regulator CsgD in cross-regulation between biofilm formation and flagellar synthesis. . J Bacteriol 193:, 2587–2597. [CrossRef] [PubMed]
    [Google Scholar]
  34. Parkinson J. S. . ( 1993; ). Signal transduction schemes of bacteria. . Cell 73:, 857–871. [CrossRef] [PubMed]
    [Google Scholar]
  35. Quail M. A. , Haydon D. J. , Guest J. R. . ( 1994; ). The pdhRaceEFlpd operon of Escherichia coli expresses the pyruvate dehydrogenase complex. . Mol Microbiol 12:, 95–104. [CrossRef] [PubMed]
    [Google Scholar]
  36. Shimada T. , Fujita N. , Maeda M. , Ishihama A. . ( 2005; ). Systematic search for the Cra-binding promoters using genomic SELEX system. . Genes Cells 10:, 907–918. [CrossRef] [PubMed]
    [Google Scholar]
  37. Shimada T. , Hirao K. , Kori A. , Yamamoto K. , Ishihama A. . ( 2007; ). RutR is the uracil/thymine-sensing master regulator of a set of genes for synthesis and degradation of pyrimidines. . Mol Microbiol 66:, 744–757. [CrossRef] [PubMed]
    [Google Scholar]
  38. Shimada T. , Yamamoto K. , Ishihama A. . ( 2009; ). Involvement of the leucine response transcription factor LeuO in regulation of the genes for sulfa drug efflux. . J Bacteriol 191:, 4562–4571. [CrossRef] [PubMed]
    [Google Scholar]
  39. Shimada T. , Bridier A. , Briandet R. , Ishihama A. . ( 2011a; ). Novel roles of LeuO in transcription regulation in E. coli: antagonistic interplay with the universal silencer H-NS. . Mol Microbiol 82:, 378–397. [CrossRef] [PubMed]
    [Google Scholar]
  40. Shimada T. , Fujita N. , Yamamoto K. , Ishihama A. . ( 2011b; ). Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources. . PLoS ONE 6:, e20081. [CrossRef] [PubMed]
    [Google Scholar]
  41. Shimada T. , Yamamoto K. , Ishihama A. . ( 2011c; ). Novel members of the Cra regulon involved in carbon metabolism in Escherichia coli . . J Bacteriol 193:, 649–659. [CrossRef] [PubMed]
    [Google Scholar]
  42. Stock J. B. , Stock A. M. , Mottonen J. M. . ( 1990; ). Signal transduction in bacteria. . Nature 344:, 395–400. [CrossRef] [PubMed]
    [Google Scholar]
  43. Teramoto J. , Yoshimura S. H. , Takeyasu K. , Ishihama A. . ( 2010; ). A novel nucleoid protein of Escherichia coli induced under anaerobiotic growth conditions. . Nucleic Acids Res 38:, 3605–3618. [CrossRef] [PubMed]
    [Google Scholar]
  44. Umezawa Y. , Ogasawara H. , Shimada T. , Kori A. , Ishihama A. . ( 2008; ). The uncharacterized YdhM is the regulator of the nemA gene, coding for N-ethylmaleimide reductase. . J Bacteriol 190:, 5890–5897. [CrossRef] [PubMed]
    [Google Scholar]
  45. Wahl A. , My L. , Dumoulin R. , Sturgis J. N. , Bouveret E. . ( 2011; ). Antagonistic regulation of dgkA and plsB genes of phospholipid synthesis by multiple stress responses in Escherichia coli . . Mol Microbiol 80:, 1260–1275. [CrossRef] [PubMed]
    [Google Scholar]
  46. Wanner B. L. , Chang B.-D. . ( 1987; ). The phoBR operon in Escherichia coli K-12. . J Bacteriol 169:, 5569–5574.[PubMed]
    [Google Scholar]
  47. Winfield M. D. , Groisman E. A. . ( 2004; ). Phenotypic differences between Salmonella and Escherichia coli resulting from the disparate regulation of homologous genes. . Proc Natl Acad Sci U S A 101:, 17162–17167. [CrossRef] [PubMed]
    [Google Scholar]
  48. Wösten M. M. , Kox L. F. , Chamnongpol S. , Soncini F. C. , Groisman E. A. . ( 2000; ). A signal transduction system that responds to extracellular iron. . Cell 103:, 113–125. [CrossRef] [PubMed]
    [Google Scholar]
  49. Yamamoto K. , Ishihama A. . ( 2005a; ). Transcriptional response of Escherichia coli to external copper. . Mol Microbiol 56:, 215–227. [CrossRef] [PubMed]
    [Google Scholar]
  50. Yamamoto K. , Ishihama A. . ( 2005b; ). Transcriptional response of Escherichia coli to external zinc. . J Bacteriol 187:, 6333–6340. [CrossRef] [PubMed]
    [Google Scholar]
  51. Yamamoto K. , Ishihama A. . ( 2006; ). Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli . . Biosci Biotechnol Biochem 70:, 1688–1695. [CrossRef] [PubMed]
    [Google Scholar]
  52. 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] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.057745-0
Loading
/content/journal/micro/10.1099/mic.0.057745-0
Loading

Data & Media loading...

Supplements

Table S1 

PDF
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