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
2020-09-29
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 Chem256:11905–11910[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 Bacteriol175:4528–4537[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 Biol2:2006, 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. Cell122:461–472 [CrossRef][PubMed]
    [Google Scholar]
  5. Bourret R. B.. ( 2010;). Receiver domain structure and function in response regulator proteins. Curr Opin Microbiol13:142–149 [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 Microbiol45:711–719 [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 Bacteriol172:6333–6338[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 A97:6640–6645 [CrossRef][PubMed]
    [Google Scholar]
  9. Egger L. A., Park H., Inouye M.. ( 1997;). Signal transduction via the histidyl-aspartyl phosphorelay. Genes Cells2:167–184 [CrossRef][PubMed]
    [Google Scholar]
  10. Froelich J. M., Tran K., Wall D.. ( 2006;). A pmrA constitutive mutant sensitizes Escherichia coli to deoxycholic acid. J Bacteriol188:1180–1183 [CrossRef][PubMed]
    [Google Scholar]
  11. Gao R., Stock A. M.. ( 2010;). Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Curr Opin Microbiol13:160–167 [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 Chem259:7994–7997[PubMed]
    [Google Scholar]
  13. Groisman E. A.. ( 2001;). The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol183:1835–1842 [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 Biochem68:1758–1767 [CrossRef][PubMed]
    [Google Scholar]
  15. Hantke K.. ( 2001;). Iron and metal regulation in bacteria. Curr Opin Microbiol4:172–177 [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 Microbiol76:1444–1460 [CrossRef][PubMed]
    [Google Scholar]
  17. Hoch J. A.. ( 2000;). Two-component and phosphorelay signal transduction. Curr Opin Microbiol3:165–170 [CrossRef][PubMed]
    [Google Scholar]
  18. Ishihama A.. ( 2009;). The Nucleoid: an Overview. EcoSal – Escherichia coli and Salmonella: Cellular and Molecular Biology 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 Rev34:628–645[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 Bacteriol181:5516–5520[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 Bacteriol187:1124–1134 [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 Bacteriol173:4851–4861[PubMed]
    [Google Scholar]
  23. Miller S. I., Ernst R. K., Bader M. W.. ( 2005;). LPS, TLR4 and infectious disease diversity. Nat Rev Microbiol3:36–46 [CrossRef][PubMed]
    [Google Scholar]
  24. Mizuno T.. ( 1998;). His-Asp phosphotransfer signal transduction. J Biochem123:555–563[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 Biochem114:350–357[PubMed]
    [Google Scholar]
  26. Nies D. H.. ( 2003;). Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev27:313–339 [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 A83:5909–5913 [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 Microbiol16:271–278 [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 Bacteriol189:4791–4799 [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 Bacteriol189:5534–5541 [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. Microbiology156:2470–2483 [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 Lett312:160–168 [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 Bacteriol193:2587–2597 [CrossRef][PubMed]
    [Google Scholar]
  34. Parkinson J. S.. ( 1993;). Signal transduction schemes of bacteria. Cell73:857–871 [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 Microbiol12:95–104 [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 Cells10:907–918 [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 Microbiol66:744–757 [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 Bacteriol191:4562–4571 [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 Microbiol82:378–397 [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 ONE6: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 Bacteriol193:649–659 [CrossRef][PubMed]
    [Google Scholar]
  42. Stock J. B., Stock A. M., Mottonen J. M.. ( 1990;). Signal transduction in bacteria. Nature344:395–400 [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 Res38:3605–3618 [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 Bacteriol190:5890–5897 [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 Microbiol80:1260–1275 [CrossRef][PubMed]
    [Google Scholar]
  46. Wanner B. L., Chang B.-D.. ( 1987;). The phoBR operon in Escherichia coli K-12. J Bacteriol169:5569–5574[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 A101:17162–17167 [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. Cell103:113–125 [CrossRef][PubMed]
    [Google Scholar]
  49. Yamamoto K., Ishihama A.. ( 2005a;). Transcriptional response of Escherichia coli to external copper. Mol Microbiol56:215–227 [CrossRef][PubMed]
    [Google Scholar]
  50. Yamamoto K., Ishihama A.. ( 2005b;). Transcriptional response of Escherichia coli to external zinc. J Bacteriol187:6333–6340 [CrossRef][PubMed]
    [Google Scholar]
  51. Yamamoto K., Ishihama A.. ( 2006;). Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli . Biosci Biotechnol Biochem70:1688–1695 [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 Chem280:1448–1456 [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...

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