1887

Abstract

Under stressful conditions, forms biofilm for survival by sensing a variety of environmental conditions. CsgD, the master regulator of biofilm formation, controls cell aggregation by directly regulating the synthesis of Curli fimbriae. In agreement of its regulatory role, as many as 14 transcription factors (TFs) have so far been identified to participate in regulation of the promoter, each monitoring a specific environmental condition or factor. In order to identify the whole set of TFs involved in this typical multi-factor promoter, we performed in this study ‘promoter-specific transcription-factor’ (PS-TF) screening using a set of 198 purified TFs (145 TFs with known functions and 53 hitherto uncharacterized TFs). A total of 48 TFs with strong binding to the promoter probe were identified, including 35 known TFs and 13 uncharacterized TFs, referred to as Y-TFs. As an attempt to search for novel regulators, in this study we first analysed a total of seven Y-TFs, including YbiH, YdcI, YhjC, YiaJ, YiaU, YjgJ and YjiR. After analysis of curli fimbriae formation, LacZ-reporter assay, Northern-blot analysis and biofilm formation assay, we identified at least two novel regulators, repressor YiaJ (renamed PlaR) and activator YhjC (renamed RcdB), of the promoter.

Funding
This study was supported by the:
  • Tomohiro SHIMADA , Ministry of Education, Culture, Sports, Science and Technology , (Award 19K06618)
  • Hiroshi OGASAWARA , Ministry of Education, Culture, Sports, Science and Technology , (Award 15K18670)
  • Hiroshi OGASAWARA , Shinshu University
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/content/journal/micro/10.1099/mic.0.000947
2020-07-10
2020-10-29
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References

  1. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2004; 2:95–108 [CrossRef][PubMed]
    [Google Scholar]
  2. Karatan E, Watnick P. Signals, regulatory networks, and materials that build and break bacterial biofilms. MMBR 2009; 73:310–347 [CrossRef]
    [Google Scholar]
  3. Wood TK. Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling. Environ Microbiol 2009; 11:1–15 [CrossRef][PubMed]
    [Google Scholar]
  4. Sharma G, Sharma S, Sharma P, Chandola D, Dang S et al. Escherichia coli biofilm: development and therapeutic strategies. J Appl Microbiol 2016; 121:309–319 [CrossRef][PubMed]
    [Google Scholar]
  5. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J et al. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 2002; 295:851–855 [CrossRef][PubMed]
    [Google Scholar]
  6. Hammar M»rten, Arnqvist A, Bian Z, Olsén A, Normark S. Expression of two csg operons is required for production of fibronectin- and Congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 1995; 18:661–670 [CrossRef]
    [Google Scholar]
  7. Robinson LS, Ashman EM, Hultgren SJ, Chapman MR. Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein. Mol Microbiol 2006; 59:870–881 [CrossRef][PubMed]
    [Google Scholar]
  8. Nenninger AA, Robinson LS, Hultgren SJ. Localized and efficient curli nucleation requires the chaperone-like amyloid assembly protein CsgF. Proc Natl Acad Sci U S A 2009; 106:900–905 [CrossRef][PubMed]
    [Google Scholar]
  9. Nenninger AA, Robinson LS, Hammer ND, Epstein EA, Badtke MP et al. Csge is a curli secretion specificity factor that prevents amyloid fibre aggregation. Mol Microbiol 2011; 81:486–499 [CrossRef][PubMed]
    [Google Scholar]
  10. Evans ML, Chapman MR. Curli biogenesis: order out of disorder. Biochim Biophys Acta 2014; 1843:1551–1558 [CrossRef]
    [Google Scholar]
  11. Shimada T, Katayama Y, Kawakita S, Ogasawara H, Nakano M et al. A novel regulator RcdA of the csgD gene encoding the master regulator of biofilm formation in Escherichia coli . Microbiologyopen 2012; 1:381–394 [CrossRef][PubMed]
    [Google Scholar]
  12. Ogasawara H, Yamamoto K, Ishihama A. Role of the biofilm master regulator CsgD in cross-regulation between biofilm formation and flagellar synthesis. J Bacteriol 2011; 193:2587–2597 [CrossRef][PubMed]
    [Google Scholar]
  13. Ishihama A. Prokaryotic genome regulation: multi-factor promoters and multi-target regulators. Proc Jpn Acad Ser B, Phys Biol Sci 2012; 88:485–508
    [Google Scholar]
  14. Dudin O, Geiselmann J, Ogasawara H, Ishihama A, Lacour S. Repression of flagellar genes in exponential phase by CsgD and CpxR, two crucial modulators of Escherichia coli biofilm formation. J Bacteriol 2014; 196:707–715 [CrossRef][PubMed]
    [Google Scholar]
  15. Prüß BM. Involvement of two-component signaling on bacterial motility and biofilm development. J Bacteriol 2017; 199:e00259–17 [CrossRef][PubMed]
    [Google Scholar]
  16. Mika F, Hengge R. Small RNAs in the control of RpoS, CsgD, and biofilm architecture of Escherichia coli . RNA Biol 2014; 11:494–507 [CrossRef][PubMed]
    [Google Scholar]
  17. Gerstel U, Park C, Römling U. Complex regulation of csgD promoter activity by global regulatory proteins. Mol Microbiol 2003; 49:639–654 [CrossRef][PubMed]
    [Google Scholar]
  18. Jubelin G, Vianney A, Beloin C, Ghigo J-M, Lazzaroni J-C et al. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli . J Bacteriol 2005; 187:2038–2049 [CrossRef][PubMed]
    [Google Scholar]
  19. Ogasawara H, Yamada K, Kori A, Yamamoto K, Ishihama A. Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors. Microbiology 2010a; 156:2470–2483 [CrossRef][PubMed]
    [Google Scholar]
  20. Ogasawara H, Yamamoto K, Ishihama A. Regulatory role of MlrA in transcription activation of csgD, the master regulator of biofilm formation in Escherichia coli . FEMS Microbiol Lett 2010b; 312:160–168 [CrossRef][PubMed]
    [Google Scholar]
  21. Ogasawara H, Ishizuka T, Yamaji K, Kato Y, Shimada T et al. Regulatory role of pyruvate-sensing BtsSR in biofilm formation by Escherichia coli K-12. FEMS Microbiol Lett 2019; 366:pil: fmz251 [CrossRef][PubMed]
    [Google Scholar]
  22. Ishihama A. Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. FEMS Microbiol Rev 2010; 34:628–645 [CrossRef][PubMed]
    [Google Scholar]
  23. Ishihama A, Shimada T, Yamazaki Y. Transcription profile of Escherichia coli: genomic SELEX search for regulatory targets of transcription factors. Nucleic Acids Res 2016; 44:2058–2074 [CrossRef][PubMed]
    [Google Scholar]
  24. Shimada T, Ogasawara H, Ishihama A. Genomic SELEX screening of regulatory targets of Escherichia coli transcription factors. Meth Mol Biol Vol. 1837, “Bacterial Chromatin”, Chapter 4; 2018 pp 49–69
  25. Shimada T, Yamazaki Y, Tanaka K, Ishihama A. The whole set of constitutive promoters recognized by RNA polymerase rpoD holoenzyme of Escherichia coli . PLoS One 2014; 9:e90447 [CrossRef][PubMed]
    [Google Scholar]
  26. Yoshida H, Shimada T, Ishihama A. Coordinated hibernation of transcriptional and translational apparatus during growth transition of Escherichia coli to stationary phase. mSystems 2018; 3:e00057–18 [CrossRef][PubMed]
    [Google Scholar]
  27. Sugino H, Usui T, Shimada T, Nakano M, Ogasawara H et al. A structural sketch of RcdA, a transcription factor controlling the master regulator of biofilm formation. FEBS Lett 2017; 591:2019–2031 [CrossRef][PubMed]
    [Google Scholar]
  28. Shimada T, Yokoyama Y, Anzai T, Yamamoto K, Ishihama A. Regulatory role of PlaR (YiaJ) for plant utilization in Escherichia coli K-12. Sci Rep 2019; 9:20415 [CrossRef][PubMed]
    [Google Scholar]
  29. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006; 2:2006.0008 [CrossRef][PubMed]
    [Google Scholar]
  30. Guzman LM, Belin D, Carson MJ, Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 1995; 177:4121–4130 [CrossRef][PubMed]
    [Google Scholar]
  31. Yamamoto K, Hirao K, Oshima T, Aiba H, Utsumi R et al. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli . J Biol Chem 2005; 280:1448–1456 [CrossRef][PubMed]
    [Google Scholar]
  32. Shimada K, Ogasawara H, Yamada K, Shimura M, Kori A et al. Screening of promoter-specific transcription factors: multiple regulators for the sdiA gene involved in cell division control and quorum sensing. Microbiology 2013; 159:2501–2512 [CrossRef][PubMed]
    [Google Scholar]
  33. Ogasawara H, Hasegawa A, Kanda E, Miki T, Yamamoto K et al. Genomic SELEX search for target promoters under the control of the PhoQP-RstBA signal relay cascade. J Bacteriol 2007a; 189:4791–4799 [CrossRef][PubMed]
    [Google Scholar]
  34. Ogasawara H, Ishida Y, Yamada K, Yamamoto K, Ishihama A. PdhR (pyruvate dehydrogenase complex regulator) controls the respiratory electron transport system in Escherichia coli . J Bacteriol 2007b; 189:5534–5541 [CrossRef][PubMed]
    [Google Scholar]
  35. Miller JH. Experiments in Molecular Genetics New York, NY: Cold Spring Harbor Laboratory Press; 1972
    [Google Scholar]
  36. Shimada T, Hirao K, Kori A, Yamamoto K, Ishihama A. RutR is the uracil/thymine-sensing master regulator of a set of genes for synthesis and degradation of pyrimidines. Mol Microbiol 2007; 66:744–757 [CrossRef][PubMed]
    [Google Scholar]
  37. Umezawa Y, Shimada T, Kori A, Yamada K, Ishihama A. The uncharacterized transcription factor YdhM is the regulator of the nemA gene, encoding N-ethylmaleimide reductase. J Bacteriol 2008; 190:5890–5897 [CrossRef][PubMed]
    [Google Scholar]
  38. Sule P, Wadhawan T, Carr NJ, Horne SM, Wolfe AJ et al. A combination of assays reveals biomass differences in biofilms formed by Escherichia coli mutants. Lett Appl Microbiol 2009; 49:299–304 [CrossRef][PubMed]
    [Google Scholar]
  39. Parker A, Cureoglu S, De Lay N, Majdalani N, Gottesman S. Alternative pathways for Escherichia coli biofilm formation revealed by sRNA overproduction. Mol Microbiol 2017; 105:309–325 [CrossRef][PubMed]
    [Google Scholar]
  40. Barnhart MM, Chapman MR. Curli biogenesis and function. Annu Rev Microbiol 2006; 60:131–147 [CrossRef][PubMed]
    [Google Scholar]
  41. Kan A, Birnbaum DP, Praveschotinunt P, Joshi NS. Congo Red Fluorescence for Rapid In Situ Characterization of Synthetic Curli Systems. Appl Environ Microbiol 2019; 85:e00434–19 [CrossRef][PubMed]
    [Google Scholar]
  42. Teramoto J, Yoshimura SH, Takeyasu K, Ishihama A. A novel nucleoid protein of Escherichia coli induced under anaerobiotic growth conditions. Nucleic Acids Res 2010; 38:3605–3618 [CrossRef][PubMed]
    [Google Scholar]
  43. Lim CJ, Lee SY, Teramoto J, Ishihama A, Yan J. The nucleoid-associated protein DAN organizes chromosomal DNA through rigid nucleoprotein filament formation in E. coli during anoxia. Nucleic Acids Res 2013; 41:746–753 [CrossRef][PubMed]
    [Google Scholar]
  44. Hadjifrangiskou M, Gu AP, Pinkner JS, Kostakioti M, Zhang EW et al. Transposon mutagenesis identifies uropathogenic Escherichia coli biofilm factors. J Bacteriol 2012; 194:6195–6205 [CrossRef][PubMed]
    [Google Scholar]
  45. Pérez-Rueda E, Collado-Vides J. The repertoire of DNA-binding transcriptional regulators in Escherichia coli K-12. Nucleic Acids Res 2000; 28:1838–1847 [CrossRef][PubMed]
    [Google Scholar]
  46. Ishihama A, Kori A, Koshio E, Yamada K, Maeda H et al. Intracellular concentrations of 65 species of transcription factors with known regulatory functions in Escherichia coli . J Bacteriol 2014; 196:2718–2727 [CrossRef][PubMed]
    [Google Scholar]
  47. Balderas-Martínez YI, Savageau M, Salgado H, Pérez-Rueda E, Morett E et al. Transcription factors in Escherichia coli prefer the holo conformation. PLoS One 2013; 8:e65723 [CrossRef][PubMed]
    [Google Scholar]
  48. Shimada T, Fujita N, Maeda M, Ishihama A. Systematic search for the Cra-binding promoters using genomic SELEX system. Genes Cells 2005; 10:907–918 [CrossRef][PubMed]
    [Google Scholar]
  49. Shimada T, Momiyama E, Yamanaka Y, Watanabe H, Yamamoto K, Ishihama A et al. Regulatory role of XynR (YagI) in catabolism of xylonate in Escherichia coli K-12. FEMS Microbiol Lett 2017; 364:fnx220 [CrossRef][PubMed]
    [Google Scholar]
  50. Yoshida H, Wada A, Shimada T, Maki Y, Ishihama A. Coordinated Regulation of Rsd and RMF for Simultaneous Hibernation of Transcription Apparatus and Translation Machinery in Stationary-Phase Escherichia coli . Front Genet 2019; 10:1153 [CrossRef][PubMed]
    [Google Scholar]
  51. Beloin C, Roux A, Ghigo JM. Escherichia coli biofilms. Curr Top Microbiol Immunol 2008; 322:249–289 [CrossRef][PubMed]
    [Google Scholar]
  52. Landini P. Cross-talk mechanisms in biofilm formation and responses to environmental and physiological stress in Escherichia coli . Res Microbiol 2009; 160:259–266 [CrossRef][PubMed]
    [Google Scholar]
  53. Maddocks SE, Oyston PCF. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 2008; 154:3609–3623 [CrossRef][PubMed]
    [Google Scholar]
  54. Yang C, Huang T-W, Wen S-Y, Chang C-Y, Tsai S-F et al. Genome-Wide PhoB binding and gene expression profiles reveal the hierarchical gene regulatory network of phosphate starvation in Escherichia coli. PLoS One 2012; 7:e47314 [CrossRef][PubMed]
    [Google Scholar]
  55. Yamanaka Y, Shimada T, Yamamoto K, Ishihama A. Transcription factor CecR (YbiH) regulates a set of genes affecting the sensitivity of Escherichia coli against cefoperazone and chloramphenicol. Microbiology 2016; 162:1253–1264 [CrossRef][PubMed]
    [Google Scholar]
  56. Gao Y, Yurkovich JT, Seo SW, Kabimoldayev I, Dräger A et al. Systematic discovery of uncharacterized transcription factors in Escherichia coli K-12 MG1655. Nucleic Acids Res 2018; 46:10682–10696 [CrossRef][PubMed]
    [Google Scholar]
  57. Ma Q, Yang Z, Pu M, Peti W, Wood TK. Engineering a novel c-di-GMP-binding protein for biofilm dispersal. Environ Microbiol 2011; 13:631–642 [CrossRef][PubMed]
    [Google Scholar]
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