1887

Abstract

The expression pattern of the genome in is controlled by regulating the utilization of a limited number of RNA polymerases between a total of 4600 genes on its genome. The distribution pattern of RNA polymerase on the genome changes after two steps of protein–protein interaction with seven sigma subunits and about 300 transcription factors (TFs). Based on a systematic search for the regulation target promoters recognized by each TF, we propose two novel concepts: each TF regulates a number of target promoters; and each promoter is regulated by many TFs. In parallel, attempts have been made to determine the intracellular concentrations of all TFs using two systems: quantitative immunoblot analysis using TF-specific antibodies; and reporter assay of TF promoter activities. The direct measurement of TF protein level has so far been published for a set of 60 regulators with known functions. This study describes the determination of growth phase-dependent expression levels of 90 TFs using the reporter assay system. The translational fusion vector was constructed from the TF promoter sequence including an N-terminal proximal TF segment and the reporter GFP. At the beginning of cell growth, high-level expression was observed only for a small number of TFs. In the exponential phase, approximately 80 % TFs are expressed, but the expressed TF species change upon transfer to the stationary phase. Significant changes in the pattern of TF expression were observed between aerobic and anaerobic conditions. The list of intracellular levels of TFs provides further understanding to the transcription regulation of the genome under various stressful conditions.

Funding
This study was supported by the:
  • Grant-in-Aid for Scientific Research (Award 25430173, 18310133 and 21241047)
  • MEXT (Award S0801037)
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.079889-0
2014-09-01
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/9/1903.html?itemId=/content/journal/micro/10.1099/mic.0.079889-0&mimeType=html&fmt=ahah

References

  1. Ades S. E. ( 2008). Regulation by destruction: design of the σE envelope stress response. Curr Opin Microbiol 11:535–540 [View Article][PubMed]
    [Google Scholar]
  2. Babu M. M., Luscombe N. M., Aravind L., Gerstein M., Teichmann S. A. ( 2004). Structure and evolution of transcriptional regulatory networks. Curr Opin Struct Biol 14:283–291 [View Article][PubMed]
    [Google Scholar]
  3. Borst D. W., Blumenthal R. M., Matthews R. G. ( 1996). Use of an in vivo titration method to study a global regulator: effect of varying Lrp levels on expression of gltBDF in Escherichia coli. J Bacteriol 178:6904–6912[PubMed]
    [Google Scholar]
  4. Browning D. F., Busby S. J. ( 2004). The regulation of bacterial transcription initiation. Nat Rev Microbiol 2:57–65 [View Article][PubMed]
    [Google Scholar]
  5. Cho B. K., Zengler K. K., Qiu Y., Park Y. S., Knight E. M., Barrett C. L., Gao Y., Palsson B. Ø. ( 2009). The transcription unit architecture of the Escherichia coli genome. Nat Biotechnol 27:1043–1049 [View Article][PubMed]
    [Google Scholar]
  6. Cortay J. C., Nègre D., Galinier A., Duclos B., Perrière G., Cozzone A. J. ( 1991). Regulation of the acetate operon in Escherichia coli: purification and functional characterization of the IclR repressor. EMBO J 10:675–679[PubMed]
    [Google Scholar]
  7. Demple B. ( 1996). Redox signaling and gene control in the Escherichia coli soxRS oxidative stress regulon – a review. Gene 179:53–57 [View Article][PubMed]
    [Google Scholar]
  8. Egan S. M., Schleif R. F. ( 1993). A regulatory cascade in the induction of rhaBAD. J Mol Biol 234:87–98 [View Article][PubMed]
    [Google Scholar]
  9. Gaudu P., Weiss B. ( 1996). SoxR, a [2Fe-2S] transcription factor, is active only in its oxidized form. Proc Natl Acad Sci U S A 93:10094–10098 [View Article][PubMed]
    [Google Scholar]
  10. Gerasimova A. V., Gelfand M. S. ( 2005). Evolution of the nadR regulon in Enterobacteriaceae. J Bioinform Comput Biol 3:1007–1019 [View Article][PubMed]
    [Google Scholar]
  11. Ginnoukos G., Ciulla D. M., Huang K., Haas B. J., Izard J., Levin J. Z., Livny J., Earl A. M., Gevers D., Yard D. V., Husbaum C., Birren B. W., Gnirke A. ( 2012). Efficient and robust RNA-seq process for cultured bacteria and complex community transcriptomes. Genome Biol 13:R23
    [Google Scholar]
  12. Gottesman S. ( 2004). The small RNA regulators of Escherichia coli: roles and mechanisms. Annu Rev Microbiol 58:303–328 [View Article][PubMed]
    [Google Scholar]
  13. Grainger D. C., Busby S. J. ( 2008). Methods for studying global patterns of DNA binding by bacterial transcription factors and RNA polymerase. Biochem Soc Trans 36:754–757 [View Article][PubMed]
    [Google Scholar]
  14. Gruber T. M., Gross C. A. ( 2003). Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57:441–466 [View Article][PubMed]
    [Google Scholar]
  15. Gunsalus R. P., Miguel A. G., Gunsalus G. L. ( 1986). Intracellular Trp repressor levels in Escherichia coli. J Bacteriol 167:272–278[PubMed]
    [Google Scholar]
  16. Habdas B. J., Smart J., Kaper J. B., Sperandio V. ( 2010). The LysR-type transcriptional regulator QseD alters type three secretion in enterohemorrhagic Escherichia coli and motility in K-12 Escherichia coli. J Bacteriol 192:3699–3712 [View Article][PubMed]
    [Google Scholar]
  17. Hanlon S. P., Hill T. K., Flavell M. A., Stringfellow J. M., Cooper R. A. ( 1997). 2-Phenylethylamine catabolism by Escherichia coli K-12: gene organization and expression. Microbiology 143:513–518 [View Article][PubMed]
    [Google Scholar]
  18. Hayashi K., Morooka N., Yamamoto Y., Fujita K., Isono K., Choi S., Ohtsubo E., Baba T., Wanner B. L. & other authors ( 2006). Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2:0007 [View Article][PubMed]
    [Google Scholar]
  19. Herring C. D., Raffaelle M., Allen T. E., Kanin E. I., Landick R., Ansari A. Z., Palsson B. O. ( 2005). Immobilization of Escherichia coli RNA polymerase and location of binding sites by use of chromatin immunoprecipitation and microarrays. J Bacteriol 187:6166–6174 [View Article][PubMed]
    [Google Scholar]
  20. Ishihama A. ( 2000). Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 54:499–518 [View Article][PubMed]
    [Google Scholar]
  21. Ishihama A. ( 2010). Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. FEMS Microbiol Rev 34:628–645[PubMed]
    [Google Scholar]
  22. Ishihama A. ( 2012). Prokaryotic genome regulation: a revolutionary paradigm. Proc Jpn Acad, Ser B, Phys Biol Sci 88:485–508 [View Article][PubMed]
    [Google Scholar]
  23. Ishihama A., Kori A., Koshio E., Yamada K., Maeda H., Shimada T., Makinoshima H., Iwata A., Fujita N. ( 2014). Intracellular concentrations of transcription factors in Escherichia coli: 65 species with known regulatory functions. J Bacteriol 169:2718–2727 . [View Article][PubMed]
    [Google Scholar]
  24. Jishage M., Ishihama A. ( 1995). Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of σ70 and σ38. J Bacteriol 177:6832–6835[PubMed]
    [Google Scholar]
  25. Jishage M., Ishihama A. ( 1997). Variation in RNA polymerase sigma subunit composition within different stocks of Escherichia coli W3110. J Bacteriol 179:959–963[PubMed]
    [Google Scholar]
  26. Jishage M., Iwata A., Ueda S., Ishihama A. ( 1996). Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of four species of sigma subunit under various growth conditions. J Bacteriol 178:5447–5451[PubMed]
    [Google Scholar]
  27. Kalivoda K. A., Steenbergen S. M., Vimr E. R., Plumbridge J. ( 2003). Regulation of sialic acid catabolism by the DNA binding protein NanR in Escherichia coli. J Bacteriol 185:4806–4815 [View Article][PubMed]
    [Google Scholar]
  28. Keseler I. M., Mackie A., Peralta-Gil M., Santos-Zavaleta A., Gama-Castro S., Bonavides-Martínez C., Fulcher C., Huerta A. M., Kothari A. & other authors ( 2013). EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res 41:Database issueD605–D612 [View Article][PubMed]
    [Google Scholar]
  29. Keyhani N. O., Roseman S. ( 1997). Wild-type Escherichia coli grows on the chitin disaccharide, N,N′-diacetylchitobiose, by expressing the cel operon. Proc Natl Acad Sci U S A 94:14367–14371 [View Article][PubMed]
    [Google Scholar]
  30. Ko M., Park C. ( 2000). H-NS-dependent regulation of flagellar synthesis is mediated by a LysR family protein. J Bacteriol 182:4670–4672 [View Article][PubMed]
    [Google Scholar]
  31. Krin E., Danchin A., Soutourina O. ( 2010). Decrypting the H-NS-dependent regulatory cascade of acid stress resistance in Escherichia coli. BMC Microbiol 10:273 [View Article][PubMed]
    [Google Scholar]
  32. Kundu T. K., Kusano S., Ishihama A. ( 1997). Promoter selectivity of Escherichia coli RNA polymerase σF holoenzyme involved in transcription of flagellar and chemotaxis genes. J Bacteriol 179:4264–4269[PubMed]
    [Google Scholar]
  33. Kurihara S., Oda S., Kato K., Kim H. G., Koyanagi T., Kumagai H., Suzuki H. ( 2005). A novel putrescine utilization pathway involves gamma-glutamylated intermediates of Escherichia coli K-12. J Biol Chem 280:4602–4608 [View Article][PubMed]
    [Google Scholar]
  34. Kurnasov O. V., Polanuyer B. M., Ananta S., Sloutsky R., Tam A., Gerdes S. Y., Osterman A. L. ( 2002). Ribosylnicotinamide kinase domain of NadR protein: identification and implications in NAD biosynthesis. J Bacteriol 184:6906–6917 [View Article][PubMed]
    [Google Scholar]
  35. Lee S. K., Newman J. D., Keasling J. D. ( 2005). Catabolite repression of the propionate catabolic genes in Escherichia coli and Salmonella enterica: evidence for involvement of the cyclic AMP receptor protein. J Bacteriol 187:2793–2800 [View Article][PubMed]
    [Google Scholar]
  36. Lim C. J., Lee S. Y., Teramoto J., Ishihama A., Yan J. ( 2013). The nucleoid-associated protein Dan organizes chromosomal DNA through rigid nucleoprotein filament formation in E. coli during anoxia. Nucleic Acids Res 41:746–753 [View Article][PubMed]
    [Google Scholar]
  37. Lundrigan M. D., Earhart C. F. ( 1984). Gene envY of Escherichia coli K-12 affects thermoregulation of major porin expression. J Bacteriol 157:262–268[PubMed]
    [Google Scholar]
  38. Luzader D. H., Clark D. E., Gonyar L. A., Kendall M. M. ( 2013). EutR is a direct regulator of genes that contribute to metabolism and virulence in enterohemorrhagic Escherichia coli O157:H7. J Bacteriol 195:4947–4953 [View Article][PubMed]
    [Google Scholar]
  39. Maeda H., Jishage M., Nomura T., Fujita N., Ishihama A. ( 2000). Two extracytoplasmic function sigma subunits, ζE and ζFecI, of Escherichia coli: promoter selectivity and intracellular levels. J Bacteriol 182:1181–1184 [View Article][PubMed]
    [Google Scholar]
  40. Martin R. G., Rosner J. L. ( 2001). The AraC transcriptional activators. Curr Opin Microbiol 4:132–137 [View Article][PubMed]
    [Google Scholar]
  41. Martínez-Antonio A., Collado-Vides J. ( 2003). Identifying global regulators in transcriptional regulatory networks in bacteria. Curr Opin Microbiol 6:482–489 [View Article][PubMed]
    [Google Scholar]
  42. Mitobe J., Yanagihara I., Ohnishi K., Yamamoto S., Ohnishi M., Ishihama A., Watanabe H. ( 2011). RodZ regulates the post-transcriptional processing of the Shigella sonnei type III secretion system. EMBO Rep 12:911–916 [View Article][PubMed]
    [Google Scholar]
  43. Mooney R. A., Davis S. E., Peters J. M., Rowland J. L., Ansari A. Z., Landick R. ( 2009). Regulator trafficking on bacterial transcription units in vivo. Mol Cell 33:97–108 [View Article][PubMed]
    [Google Scholar]
  44. Ogasawara H., Yamada Y., Kori A., Yamamoto K., Ishihama A. ( 2010). The E. coli csgD promoter: interplay between eight transcription factors. Microbiology 156:2470–2483 [View Article][PubMed]
    [Google Scholar]
  45. Oh M.-K., Rohlin L., Kao K. C., Liao J. C. ( 2002). Global expression profiling of acetate-grown Escherichia coli. J Biol Chem 277:13175–13183 [View Article][PubMed]
    [Google Scholar]
  46. Overton T. W., Griffiths L., Patel M. D., Hobman J. L., Penn C. W., Cole J. A., Constantinidou C. ( 2006). Microarray analysis of gene regulation by oxygen, nitrate, nitrite, FNR, NarL and NarP during anaerobic growth of Escherichia coli: new insights into microbial physiology. Biochem Soc Trans 34:104–107 [View Article][PubMed]
    [Google Scholar]
  47. Paget M. S., Helmann J. D. ( 2003). The σ70 family of sigma factors. Genome Biol 4:203 [View Article][PubMed]
    [Google Scholar]
  48. Patten C. L., Kirchhof M. G., Schertzberg M. R., Morton R. A., Schellhorn H. E. ( 2004). Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics 272:580–591 [View Article][PubMed]
    [Google Scholar]
  49. Pellicer M. T., Fernandez C., Badía J., Aguilar J., Lin E. C. C., Baldom L. ( 1999). 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 [View Article][PubMed]
    [Google Scholar]
  50. Pérez-Rueda E., Collado-Vides J. ( 2000). The repertoire of DNA-binding transcriptional regulators in Escherichia coli K-12. Nucleic Acids Res 28:1838–1847 [View Article][PubMed]
    [Google Scholar]
  51. Phadtare S., Inouye M. ( 2004). Genome-wide transcriptional analysis of the cold shock response in wild-type and cold-sensitive, quadruple-csp-deletion strains of Escherichia coli. J Bacteriol 186:7007–7014 [View Article][PubMed]
    [Google Scholar]
  52. Raghavan R., Sage A., Ochman H. ( 2011). Genome-wide identification of transcription start sites yields a novel thermosensing RNA and new cyclic AMP receptor protein-regulated genes in Escherichia coli. J Bacteriol 193:2871–2874 [View Article][PubMed]
    [Google Scholar]
  53. Ren D., Bedzyk L. A., Thomas S. M., Ye R. W., Wood T. K. ( 2004). Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64:515–524 [View Article][PubMed]
    [Google Scholar]
  54. Richmond C. S., Glasner J. D., Mau R., Jin H., Blattner F. R. ( 1999). Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res 27:3821–3835 [View Article][PubMed]
    [Google Scholar]
  55. Riley M., Abe T., Arnaud M. B., Berlyn M. K. B., Blattner F. R., Chaudhuri R. R., Glasner J. D., Horiuchi T., Keseler I. M. & other authors ( 2006). Escherichia coli K-12: a cooperatively developed annotation snapshot–2005. Nucleic Acids Res 34:1–9 [View Article][PubMed]
    [Google Scholar]
  56. Riordan J. T., Tietjen J. A., Walsh C. W., Gustafson J. E., Whittam T. S. ( 2010). Inactivation of alternative sigma factor 54 (RpoN) leads to increased acid resistance, and alters locus of enterocyte effacement (LEE) expression in Escherichia coli O157 : H7. Microbiology 156:719–730 [View Article][PubMed]
    [Google Scholar]
  57. Salgado H., Peralta-Gil M., Gama-Castro S., Santos-Zavaleta A., Muñiz-Rascado L., García-Sotelo J. S., Weiss V., Solano-Lira H., Martínez-Flores I. & other authors ( 2013). RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more. Nucleic Acids Res 41:Database issueD203–D213 [View Article][PubMed]
    [Google Scholar]
  58. Sawers G. ( 1998). The anaerobic degradation of L-serine and L-threonine in enterobacteria: networks of pathways and regulatory signals. Arch Microbiol 171:1–5 [View Article][PubMed]
    [Google Scholar]
  59. Sawers G. ( 2001). A novel mechanism controls anaerobic and catabolite regulation of the Escherichia coli tdc operon. Mol Microbiol 39:1285–1298 [View Article][PubMed]
    [Google Scholar]
  60. Shimada T., Makinoshima H., Ogawa Y., Miki T., Maeda M., Ishihama A. ( 2004). Classification and strength measurement of stationary-phase promoters by use of a newly developed promoter cloning vector. J Bacteriol 186:7112–7122 [View Article][PubMed]
    [Google Scholar]
  61. 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 [View Article][PubMed]
    [Google Scholar]
  62. Shimada K., Ogasawara H., Yamada K., Shimura M., Kori A., Shimada T., Yamanaka Y., Yamamoto K., Ishihama A. ( 2013). Screening of promoter-specific transcription factors: multiple regulators for the sdiA gene involved in cell division control and quorum sensing. Microbiology 159:2501–2512 [View Article][PubMed]
    [Google Scholar]
  63. Shiomi D., Sakai M., Niki H. ( 2008). Determination of bacterial rod shape by a novel cytoskeletal membrane protein. EMBO J 27:3081–3091 [View Article][PubMed]
    [Google Scholar]
  64. Song S., Park C. ( 1997). Organization and regulation of the D-xylose operons in Escherichia coli K-12: XylR acts as a transcriptional activator. J Bacteriol 179:7025–7032[PubMed]
    [Google Scholar]
  65. 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 [View Article][PubMed]
    [Google Scholar]
  66. Tramonti A., Visca P., De Canio M., Falconi M., De Biase D. ( 2002). Functional characterization and regulation of gadX, a gene encoding an AraC/XylS-like transcriptional activator of the Escherichia coli glutamic acid decarboxylase system. J Bacteriol 184:2603–2613 [View Article][PubMed]
    [Google Scholar]
  67. Tucker D. L., Tucker N., Ma Z., Foster J. W., Miranda R. L., Cohen P. S., Conway T. ( 2003). Genes of the GadX-GadW regulon in Escherichia coli. J Bacteriol 185:3190–3201 [View Article][PubMed]
    [Google Scholar]
  68. Typas A., Becker G., Hengge R. ( 2007). The molecular basis of selective promoter activation by the σS subunit of RNA polymerase. Mol Microbiol 63:1296–1306 [View Article][PubMed]
    [Google Scholar]
  69. Wiame E., Delpierre G., Collard F., Van Schaftingen E. ( 2002). Identification of a pathway for the utilization of the Amadori product fructoselysine in Escherichia coli. J Biol Chem 277:42523–42529 [View Article][PubMed]
    [Google Scholar]
  70. Yamamoto K. ( 2014). The hierarchic network of metal-response transcription factors in Escherichia coli. Biosci Biotechnol Biochem 78:737–747 [View Article][PubMed]
    [Google Scholar]
  71. Zhang X. S., García-Contreras R., Wood T. K. ( 2008). Escherichia coli transcription factor YncC (McbR) regulates colanic acid and biofilm formation by repressing expression of periplasmic protein YbiM (McbA). ISME J 2:615–631 [View Article][PubMed]
    [Google Scholar]
  72. Zheng M., Wang X., Templeton L. J., Smulski D. R., LaRossa R. A., Storz G. ( 2001). DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.079889-0
Loading
/content/journal/micro/10.1099/mic.0.079889-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

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