1887

Abstract

Genomic SELEX (systematic evolution of ligands by exponential enrichment) screening was performed for identification of the binding site of YbiH, an as yet uncharacterized TetR-family transcription factor, on the genome. YbiH was found to be a unique single-target regulator that binds within the intergenic spacer located between the divergently transcribed and operons. YbhG is an inner membrane protein and YbhFSR forms a membrane-associated ATP-binding cassette (ABC) transporter while RhlE is a ribosome-associated RNA helicase. Gel shift assay and DNase footprinting analyses indicated one clear binding site of YbiH, including a complete palindromic sequence of AATTAGTT—AACTAATT. An reporter assay indicated repression of the operon and activation of the operon by YbiH. After phenotype microarray screening, YbiH was indicated to confer resistance to chloramphenicol and cefazoline (a first-generation cephalosporin). A systematic survey of the participation of each of the predicted YbiH-regulated genes in the antibiotic sensitivity indicated involvement of the YbhFSR ABC-type transporter in the sensitivity to cefoperazone (a third-generation cephalosporin) and of the membrane protein YbhG in the control of sensitivity to chloramphenicol. Taken together with the growth test in the presence of these two antibiotics and transcription assay, it was concluded that the hitherto uncharacterized YbiH regulates transcription of both the bidirectional transcription units, the operon and the gene, which altogether are involved in the control of sensitivity to cefoperazone and chloramphenicol. We thus propose to rename YbiH as CecR (regulator of cefoperazone and chloramphenicol sensitivity).

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2016-07-01
2019-11-17
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References

  1. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K. A., Tomita M., Wanner B. L. et al. 2006; Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol2:2006–2008 [CrossRef][PubMed]
    [Google Scholar]
  2. Blattner F. R., Plunkett G., Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K. et al. 1997; The complete genome sequence of Escherichia coli K-12. Science277:1453–1462 [CrossRef][PubMed]
    [Google Scholar]
  3. Blouin K., Walker S. G., Smit J., Turner R.. 1996; Characterization of in vivo Reporter systems for gene expression and biosensor applications based on luxAB luciferase genes. Appl Environ Microbiol62:2013–2021[PubMed]
    [Google Scholar]
  4. Bochner B. R., Gadzinski P., Panomitros E.. 2001; Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. Genome Res11:1246–1255 [CrossRef][PubMed]
    [Google Scholar]
  5. Bulkley D., Innis C. A., Blaha G., Steitz T. A.. 2010; Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proc Natl Acad Sci U S A107:17158–17163 [CrossRef][PubMed]
    [Google Scholar]
  6. Charollais J., Pflieger D., Vinh J., Dreyfus M., Iost I.. 2003; The DEAD-box RNA helicase SrmB is involved in the assembly of 50S ribosomal subunits in Escherichia coli. Mol Microbiol48:1253–1265[CrossRef]
    [Google Scholar]
  7. Charollais J., Dreyfus M., Iost I.. 2004; CsdA, a cold-shock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit. Nucleic Acids Res32:2751–2759 [CrossRef][PubMed]
    [Google Scholar]
  8. Daley D. O., Rapp M., Granseth E., Melén K., Drew D., von Heijne G.. 2005; Global topology analysis of the Escherichia coli inner membrane proteome. Science308:1321–1323 [CrossRef][PubMed]
    [Google Scholar]
  9. Dunkle J. A., Xiong L., Mankin A. S., Cate J. H.. 2010; Structures of the Escherichia coli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proc Natl Acad Sci U S A107:17152–17157 [CrossRef][PubMed]
    [Google Scholar]
  10. Ellington A. D., Szostak J. W.. 1990; In vitro selection of RNA molecules that bind specific ligands. Nature346:818–822 [CrossRef][PubMed]
    [Google Scholar]
  11. Fujita N., Ishihama A.. 1996; Reconstitution of RNA polymerase. In RNA Polymerase and Associated Factors (Methods in Enzymology vol. 273) pp.121–130 Edited by Adhya S.. New York, NY: Academic Press;[CrossRef]
    [Google Scholar]
  12. Hansen J. L., Moore P. B., Steitz T. A.. 2003; Structures of five antibiotics bound at the peptidyl transferase center of the large ribosomal subunit. J Mol Biol330:1061–1075[CrossRef]
    [Google Scholar]
  13. Hayashi K., Morooka N., Yamamoto Y., Fujita K., Isono K., Choi S., Ohtsubo E., Baba T., Wanner B. L. et al. 2006; Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol2:0007 [CrossRef][PubMed]
    [Google Scholar]
  14. Hirakawa H., Takumi-Kobayashi A., Theisen U., Hirata T., Nishino K., Yamaguchi A.. 2008; AcrS/EnvR represses expression of the acrAB multidrug efflux genes in Escherichia coli. J Bacteriol190:6276–6279 [CrossRef][PubMed]
    [Google Scholar]
  15. Iost I., Dreyfus M.. 2006; DEAD-box RNA helicases in Escherichia coli. Nucleic Acids Res34:489–4197 [CrossRef]
    [Google Scholar]
  16. Ishihama A.. 2000; Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol54:499–518 [CrossRef][PubMed]
    [Google Scholar]
  17. Ishihama A.. (2009); The nucleoid: an overview. In EcoSal—Escherichia coli and Salmonella: Cellular and Molecular Biology Edited by Boek A., Curtiss R., Kaper J. B., Karp P. D., Neidhardt F. C., Nystrom T., Slauch J. M., Squires C. L., Ussery D.. Washington, DC: ASM Press;
    [Google Scholar]
  18. Ishihama A.. 2010; Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. FEMS Microbiol Rev34:628–645 [CrossRef][PubMed]
    [Google Scholar]
  19. Ishihama A.. 2012; Prokaryotic genome regulation: a revolutionary paradigm. Proc Jpn Acad Ser B Phys Biol Sci88:485–508[PubMed][CrossRef]
    [Google Scholar]
  20. Ishihama A., Kori A., Koshio E., Yamada K., Maeda H., Shimada T., Makinoshima H., Iwata A., Fujita N.. 2014; Intracellular concentrations of 65 species of transcription factors with known regulatory functions in Escherichia coli. J Bacteriol196:2718–2727 [CrossRef][PubMed]
    [Google Scholar]
  21. Ishihama A., Shimada T., Yamazaki Y.. 2016; Transcription profile of Escherichia coli: genomic SELEX search for regulatory targets of transcription factors. Nucleic Acids Res44:2058–2074 [CrossRef][PubMed]
    [Google Scholar]
  22. Jagessar K. L., Jain C.. 2010; Functional and molecular analysis of Escherichia coli strains lacking multiple DEAD-box helicases. RNA16:1386–1392[CrossRef]
    [Google Scholar]
  23. Jain C.. 2008; The E. coli RhlE RNA helicase regulates the function of related RNA helicases during ribosome assembly. RNA14:381–389 [CrossRef][PubMed]
    [Google Scholar]
  24. Jishage M., Ishihama A.. 1997; Variation in RNA polymerase sigma subunit composition within different stocks of Escherichia coli W3110. J Bacteriol179:959–963[PubMed][CrossRef]
    [Google Scholar]
  25. Lee J. O., Cho K. S., Kim O. B.. 2014; Overproduction of AcrR increases organic solvent tolerance mediated by modulation of SoxS regulon in Escherichia coli. Appl Microbiol Biotechnol98:8763–8773[CrossRef]
    [Google Scholar]
  26. Levy S. B.. 2002; Active efflux, a common mechanism for biocide and antibiotic resistance. J Appl Microb92:65S–71S[CrossRef]
    [Google Scholar]
  27. Li M., Gu R., Su C. C., Routh M. D., Harris K. C., Jewell E. S., McDermott G., Yu E. W.. 2007; Crystal structure of the transcriptional regulator AcrR from Escherichia coli. J Mol Biol374:591–603 [CrossRef][PubMed]
    [Google Scholar]
  28. Ma D., Cook D. N., Hearst J. E., Nikaido H.. 1994; Efflux pumps and drug resistance in Gram-negative bacteria. Trends Microbiol2:489–493 [CrossRef][PubMed]
    [Google Scholar]
  29. Ma D., Alberti M., Lynch C., Nikaido H., Hearst J. E.. 1996; The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol Micriobiol19:101–112[CrossRef]
    [Google Scholar]
  30. Mankin A. S., Garrett R. A.. 1991; Chloramphenicol resistance mutations in the single 23S rRNA gene of the archaeon Halobacterium halobium. J Bacteriol173:3559–3563[PubMed][CrossRef]
    [Google Scholar]
  31. Moussatova A., Kandt C., O'Mara M. L., Tieleman D. P., O’Hara M. L.. 2008; ATP-binding cassette transporters in Escherichia coli. Biochim Biophys Acta1778:1757–1771 [CrossRef][PubMed]
    [Google Scholar]
  32. Ogasawara H., Ishida Y., Yamada K., Yamamoto K., Ishihama A.. 2007; PdhR (pyruvate dehydrogenase complex regulator) controls the respiratory electron transport system in Escherichia coli. J Bacteriol189:5534–5541 [CrossRef][PubMed]
    [Google Scholar]
  33. Ogasawara H., Ohe S., Ishihama A.. 2015; Role of transcription factor NimR (YeaM) in sensitivity control of Escherichia coli to 2-nitroimidazole. FEMS Microbiol Lett362:1–8 [CrossRef][PubMed]
    [Google Scholar]
  34. Paulsen I. T., Brown M. H., Skurray R. A.. 1996; Proton-dependent multidrug efflux systems. Microbiol Mol Biol Rev60:575–608[PubMed]
    [Google Scholar]
  35. Putman M., van Veen H. W., Konings W. N.. 2000; Molecular properties of bacterial multidrug transporters. Microbiol Mol Biol Res64:672–693[CrossRef]
    [Google Scholar]
  36. Ramos J. L., Martínez-Bueno M., Molina-Henares A. J., Terán W., Watanabe K., Zhang X., Gallegos M. T., Brennan R., Tobes R.. 2005; The TetR family of transcriptional repressors. Microbiol Mol Biol Rev69:326–356[CrossRef]
    [Google Scholar]
  37. Riley M., Abe T., Arnaud M. B., Berlyn M. K., Blattner F. R., Chaudhuri R. R., Glasner J. D., Horiuchi T., Keseler I. M. et al. 2006; Escherichia coli K-12: a cooperatively developed annotation snapshot 2005. Nucleic Acids Res34:1–9 [CrossRef][PubMed]
    [Google Scholar]
  38. Schlünzen F., Zarivach R., Harms J., Bashan A., Tocilj A., Albrecht R., Yonath A., Franceschi F.. 2001; Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature413:814–821 [CrossRef][PubMed]
    [Google Scholar]
  39. 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]
  40. 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 Microbiol82:376–397[CrossRef]
    [Google Scholar]
  41. 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
    [Google Scholar]
  42. Shimada T., Yamazaki K., Ishihama A.. 2013; Novel regulator PgrR for switch control of peptidoglycan recycling in Escherichia coli. Genes Cells18:123–134 [CrossRef][PubMed]
    [Google Scholar]
  43. Shimada T., Yamazaki Y., Tanaka K., Ishihama A.. 2014; The whole set of constitutive promoters recognized by RNA polymerase RpoD holoenzyme of Escherichia coli. PLoS One9:e90447 [CrossRef][PubMed]
    [Google Scholar]
  44. Su C. C., Rutherford D. J., Yu E. W.. 2007; Characterization of the multidrug efflux regulator AcrR from Escherichia coli. Biochem Biophys Res Commun361:85–90 [CrossRef][PubMed]
    [Google Scholar]
  45. 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]
    [Google Scholar]
  46. Theodoulou F. L., Kerr I. D.. 2015; ABC transporter research: going strong 40 years on. Biochem Soc Trans43:1033–1040 [CrossRef][PubMed]
    [Google Scholar]
  47. Trubetskoy D., Proux F., Allemand F., Dreyfus M., Iost I.. 2009; SrmB, a DEAD-box helicase involved in Escherichia coli ribosome assembly, is specifically targeted to 23S rRNA in vivo. Nucleic Acids Res37:6540–6549 [CrossRef][PubMed]
    [Google Scholar]
  48. Tuerk C., Gold L.. 1990; Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science249:505–510[PubMed][CrossRef]
    [Google Scholar]
  49. Wilson D. N.. 2009; The A–Z of bacterial translation inhibitors. Crit Rev Biochem Mol Biol44:393–433[CrossRef]
    [Google Scholar]
  50. Wolfe A. D., Hahn F. E.. 1965; Mode of action of chloramphenicol: effects of chloramphenicol upon a ribosomal amino acid polymerization system and its binding to bacterial ribosome. Biochim Biophys Acta95:146–155[PubMed][CrossRef]
    [Google Scholar]
  51. 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]
  52. Yamanaka Y., Oshima T., Ishihama A., Yamamoto K.. 2014; Characterization of the YdeO regulon in Escherichia coli. PLoS One9:e111962 [CrossRef][PubMed]
    [Google Scholar]
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