Activation and repression of a σn-dependent promoter naturally lacking upstream activation sequences

Molecular Microbiology

Volumn 73, Issue 3, 2009, Pages 419-433

  Porrúa, Odil ^a   García González, Vicente ^a,c   Santero, Eduardo ^a   Shingler, Victoria ^b   Govantes, Fernando ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b UMEÅ UNIVERSITY   (Sweden)

^c ORYZON GENOMICS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; ATZR PROTEIN; BACTERIAL PROTEIN; BETA GALACTOSIDASE; CYANURIC ACID; DNA BINDING PROTEIN; NITROGEN; RNA POLYMERASE; SERINE; SIGMA FACTOR; UNCLASSIFIED DRUG; SIGMA FACTOR RPON;

ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; BINDING SITE; DNA BINDING; ENZYME ACTIVITY; ENZYME ASSAY; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN PURIFICATION; PSEUDOMONAS; PSEUDOMONAS PUTIDA; TRANSCRIPTION REGULATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; TRANSCRIPTION INITIATION;

PSEUDOMONAS SP. ADP;

BINDING SITES; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; PROMOTER REGIONS, GENETIC; PSEUDOMONAS; RNA POLYMERASE SIGMA 54; TRANSCRIPTIONAL ACTIVATION;

EID: 67651219392     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06779.x     Document Type: Article

References (77)

1. Arcondeguy, T., Jack, R. Merrick, M. (2001) P(II) signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65 : 80 105.
2. Bao, Y., Lies, D.P., Fu, H. Roberts, G.P. (1991) An improved Tn7-based system for the single-copy insertion of cloned genes into the chromosomes of Gram-negative bacteria. Gene 109 : 167 168.
3. Beck, L.L., Smith, T.G. Hoover, T.R. (2007) Look, no hands! Unconventional transcriptional activators in bacteria. Trends Microbiol 15 : 530 537.
4. Belitsky, B.R., Janssen, P.J. Sonenshein, A.L. (1995) Sites required for GltC-dependent regulation of Bacillus subtilis glutamate synthase expression. J Bacteriol 177 : 5686 5695.
5. Belitsky, B.R. Sonenshein, A.L. (1999) An enhancer element located downstream of the major glutamate dehydrogenase gene of Bacillus subtilis. Proc Natl Acad Sci USA 96 : 10290 10295.
6. Berger, D.K., Narberhaus, F. Kustu, S. (1994) The isolated catalytic domain of NIFA, a bacterial enhancer-binding protein, activates transcription in vitro: activation is inhibited by NIFL. Proc Natl Acad Sci USA 91 : 103 107.
7. Berger, D.K., Narberhaus, F., Lee, H.S. Kustu, S. (1995) In vitro studies of the domains of the nitrogen fixation regulatory protein NIFA. J Bacteriol 177 : 191 199.
8. 54-promoter discrimination and regulation by ppGpp and DksA. J Biol Chem 284 : 828 838.
9. 54-RNA polymerase holoenzyme. J Bacteriol 186 : 4535 4542.
10. Buck, M. Cannon, W. (1989) Mutations in the RNA polymerase recognition sequence of the Klebsiella pneumoniae nifH promoter permitting transcriptional activation in the absence of NifA binding to upstream activator sequences. Nucleic Acids Res 17 : 2597 2612.
11. Buck, M., Gallegos, M.T., Studholme, D.J., Guo, Y. Gralla, J.D. (2000) The bacterial enhancer-dependent sigma(54) (sigma(N)) transcription factor. J Bacteriol 182 : 4129 4136.
12. Burtnick, M.N., Downey, J.S., Brett, P.J., Boylan, J.A., Frye, J.G., Hoover, T.R. Gherardini, F.C. (2007) Insights into the complex regulation of rpoS in Borrelia burgdorferi. Mol Microbiol 65 : 277 293.
13. Cannon, W., Missailidis, S., Austin, S., Moore, M., Drake, A. Buck, M. (1996) Purification and activities of the Rhodobacter capsulatus RpoN (sigma N) protein. Mol Microbiol 21 : 233 245.
14. 54 regulon (sigmulon) of Pseudomonas putida. Environ Microbiol 5 : 1281 1293.
15. Drummond, M., Clements, J., Merrick, M. Dixon, R. (1983) Positive control and autogenous regulation of the nifLA promoter in Klebsiella pneumoniae. Nature 301 : 302 307.
16. Elliott, T. Geiduschek, E.P. (1984) Defining a bacteriophage T4 late promoter: absence of a '-35' region. Cell 36 : 211 219.
17. Espinosa-Urgel, M., Salido, A. Ramos, J.L. (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182 : 2363 2369.
18. Feng, J., Goss, T.J., Bender, R.A. Ninfa, A.J. (1995) Repression of the Klebsiella aerogenes nac promoter. J Bacteriol 177 : 5535 5538.
19. Figurski, D.H. Helinski, D.R. (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci USA 76 : 1648 1652.
20. Franklin, F.C., Bagdasarian, M., Bagdasarian, M.M. Timmis, K.N. (1981) Molecular and functional analysis of the TOL plasmid pWWO from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta cleavage pathway. Proc Natl Acad Sci USA 78 : 7458 7462.
21. García-González, V., Govantes, F., Porrúa, O. Santero, E. (2005) Regulation of the Pseudomonas sp. strain ADP cyanuric acid degradation operon. J Bacteriol 187 : 155 167.
22. Govantes, F., Molina-López, J.A. Santero, E. (1996) Mechanism of coordinated synthesis of the antagonistic regulatory proteins NifL and NifA of Klebsiella pneumoniae. J Bacteriol 178 : 6817 6823.
23. Hager, D.A., Jin, D.J. Burgess, R.R. (1990) Use of Mono Q high-resolution ion-exchange chromatography to obtain highly pure and active Escherichia coli RNA polymerase. Biochemistry 29 : 7890 7894.
24. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166 : 557 580.
25. Hervás, A.B., Canosa, I. Santero, E. (2008) Transcriptome analysis of Pseudomonas putida in response to nitrogen availability. J Bacteriol 190 : 416 420.
26. Hoover, T.R., Santero, E., Porter, S. Kustu, S. (1990) The integration host factor stimulates interaction of RNA polymerase with NIFA, the transcriptional activator for nitrogen fixation operons. Cell 63 : 11 22.
27. Huala, E. Ausubel, F.M. (1989) The central domain of Rhizobium meliloti NifA is sufficient to activate transcription from the R. meliloti nifH promoter. J Bacteriol 171 : 3354 3365.
28. Huala, E., Stigter, J. Ausubel, F.M. (1992) The central domain of Rhizobium leguminosarum DctD functions independently to activate transcription. J Bacteriol 174 : 1428 1431.
29. Inoue, H., Nojima, H. Okayama, H. (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96 : 23 28.
30. Johansson, L.U., Solera, D., Bernardo, L.M., Moscoso, J.A. Shingler, V. (2008) Sigma(54)-RNA polymerase controls sigma(70)-dependent transcription from a non-overlapping divergent promoter. Mol Microbiol 70 : 709 723.
31. Jyot, J., Dasgupta, N. Ramphal, R. (2002) FleQ, the major flagellar gene regulator in Pseudomonas aeruginosa, binds to enhancer sites located either upstream or atypically downstream of the RpoN binding site. J Bacteriol 184 : 5251 5260.
32. Klose, K.E., Weiss, D.S. Kustu, S. (1993) Glutamate at the site of phosphorylation of nitrogen-regulatory protein NTRC mimics aspartyl-phosphate and activates the protein. J Mol Biol 232 : 67 78.
33. Koch, B., Jensen, L.E. Nybroe, O. (2001) Apanel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral chromosomal site. J Microbiol Methods 45 : 187 195.
34. Kovacikova, G. Skorupski, K. (2001) Overlapping binding sites for the virulence gene regulators AphA, AphB and cAMP-CRP at the Vibrio cholerae tcpPH promoter. Mol Microbiol 41 : 393 407.
35. Kustu, S., Santero, E., Keener, J., Popham, D. Weiss, D. (1989) Expression of sigma 54 (ntrA)-dependent genes is probably united by a common mechanism. Microbiol Rev 53 : 367 376.
36. Mandelbaum, R.T., Wackett, L.P. Allan, D.L. (1993) Mineralization of the s-triazine ring of atrazine by stable bacterial mixed cultures. Appl Environ Microbiol 59 : 1695 1701.
37. Mao, X.J., Huo, Y.X., Buck, M., Kolb, A. Wang, Y.P. (2007) Interplay between CRP-cAMP and PII-Ntr systems forms novel regulatory network between carbon metabolism and nitrogen assimilation in Escherichia coli. Nucleic Acids Res 35 : 1432 1440.
38. Martinez, B., Tomkins, J., Wackett, L.P., Wing, R. Sadowsky, M.J. (2001) Complete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP. J Bacteriol 183 : 5684 5697.
39. Martínez, M., Brito, B., Imperial, J. Ruiz-Argüeso, T. (2004) Characterization of a new internal promoter (P3) for Rhizobium leguminosarum hydrogenase accessory genes hupGHIJ. Microbiology 150 : 665 675.
40. Martin-Verstraete, I., Stulke, J., Klier, A. Rapoport, G. (1995) Two different mechanisms mediate catabolite repression of the Bacillus subtilis levanase operon. J Bacteriol 177 : 6919 6927.
41. Merrick, M.J. Edwards, R.A. (1995) Nitrogen control in bacteria. Microbiol Rev 59 : 604 622.
42. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
43. Molina-Lopez, J.A. Santero, E. (1999) An artificial enhancer with multiple response elements stimulates prokaryotic transcriptional activation medicated by various regulatory proteins. Mol Gen Genet 262 : 291 301.
44. Morett, E. Buck, M. (1988) NifA-dependent in vivo protection demonstrates that the upstream activator sequence of nif promoters is a protein binding site. Proc Natl Acad Sci USA 85 : 9401 9405.
45. 54 with the Klebsiella pneumoniae and Rhizobium meliloti nifH promoters. The role of NifA in the formation of an open promoter complex. J Mol Biol 210 : 65 77.
46. Morett, E. Segovia, L. (1993) The sigma 54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains. J Bacteriol 175 : 6067 6074.
47. Ninfa, A.J., Reitzer, L.J. Magasanik, B. (1987) Initiation of transcription at the bacterial glnAp2 promoter by purified E. coli components is facilitated by enhancers. Cell 50 : 1039 1046.
48. Ostrowski, J. Kredich, N.M. (1991) Negative autoregulation of cysB in Salmonella typhimurium: in vitro interactions of CysB protein with the cysB promoter. J Bacteriol 173 : 2212 2218.
49. Parsek, M.R., Shinabarger, D.L., Rothmel, R.K. Chakrabarty, A.M. (1992) Roles of CatR and cis,cis-muconate in activation of the catBC operon, which is involved in benzoate degradation in Pseudomonas putida. J Bacteriol 174 : 7798 7806.
50. Poggio, S., Osorio, A., Dreyfus, G. Camarena, L. (2005) The flagellar hierarchy of Rhodobacter sphaeroides is controlled by the concerted action of two enhancer-binding proteins. Mol Microbiol 58 : 969 983.
51. Popham, D.L., Szeto, D., Keener, J. Kustu, S. (1989) Function of a bacterial activator protein that binds to transcriptional enhancers. Science 243 : 629 635.
52. Porrúa, O., García-Jaramillo, M., Santero, E. Govantes, F. (2007) The LysR-type regulator AtzR binding site: DNA sequences involved in activation, repression and cyanuric acid-dependent repositioning. Mol Microbiol 66 : 410 427.
53. Porter, S.C., North, A.K., Wedel, A.B. Kustu, S. (1993) Oligomerization of NTRC at the glnA enhancer is required for transcriptional activation. Genes Dev 7 : 2258 2273.
54. Reitzer, L. (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57 : 155 176.
55. Reitzer, L.J. Magasanik, B. (1986) Transcription of glnA in E. coli is stimulated by activator bound to sites far from the promoter. Cell 45 : 785 792.
56. Reitzer, L. Schneider, B.L. (2001) Metabolic context and possible physiological themes of sigma(54)-dependent genes in Escherichia coli. Microbiol Mol Biol Rev 65 : 422 444.
57. Rojo, F. (1999) Repression of transcription initiation in bacteria. J Bacteriol 181 : 2987 2991.
58. Rojo, F. (2001) Mechanisms of transcriptional repression. Curr Opin Microbiol 4 : 145 151.
59. Sambrook, J., Russell, D.W. Russell, D. (2000) Molecular Cloning, a Laboratory Manual. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
60. Schell, M.A. (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47 : 597 626.
61. Schmitz, G., Nikaido, K. Ames, G.F. (1988) Regulation of a transport operon promoter in Salmonella typhimurium: identification of sites essential for nitrogen regulation. Mol Gen Genet 215 : 107 117.
62. Schneider, B.L., Shiau, S.P. Reitzer, L.J. (1991) Role of multiple environmental stimuli in control of transcription from a nitrogen-regulated promoter in Escherichia coli with weak or no activator-binding sites. J Bacteriol 173 : 6355 6363.
63. Schumacher, J., Joly, N., Rappas, M., Zhang, X. Buck, M. (2006) Structures and organisation of AAA+ enhancer binding proteins in transcriptional activation. J Struct Biol 156 : 190 199.
64. Shingler, V. (2003) Integrated regulation in response to aromatic compounds: from signal sensing to attractive behaviour. Environ Microbiol 5 : 1226 1241.
65. Simons, R.W., Houman, F. Kleckner, N. (1987) Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53 : 85 96.
66. 54-dependent transcriptional activators. J Bacteriol 185 : 1757 1767.
67. Toledano, M.B., Kullik, I., Trinh, F., Baird, P.T., Schneider, T.D. Storz, G. (1994) Redox-dependent shift of OxyR-DNA contacts along an extended DNA-binding site: a mechanism for differential promoter selection. Cell 78 : 897 909.
68. Tropel, D. van der Meer, J.R. (2004) Bacterial transcriptional regulators for degradation pathways of aromatic compounds. Microbiol Mol Biol Rev 68 : 474 500.
69. 54 RNA polymerase and blocks transcriptional activation of the dctA promoter. EMBO J 17 : 786 796.
70. Wedel, A., Weiss, D.S., Popham, D., Droge, P. Kustu, S. (1990) A bacterial enhancer functions to tether a transcriptional activator near a promoter. Science 248 : 486 490.
71. Wek, R.C. Hatfield, G.W. (1988) Transcriptional activation at adjacent operators in the divergent-overlapping ilvY and ilvC promoters of Escherichia coli. J Mol Biol 203 : 643 663.
72. 54 promoter-specificity factor. Mol Microbiol 68 : 538 546.
73. Wikstrom, P., O'Neill, E., Ng, L.C. Shingler, V. (2001) The regulatory N-terminal region of the aromatic-responsive transcriptional activator DmpR constrains nucleotide-triggered multimerisation. J Mol Biol 314 : 971 984.
74. Wu, S.Q., Chai, W., Lin, J.T. Stewart, V. (1999) General nitrogen regulation of nitrate assimilation regulatory gene nasR expression in Klebsiella oxytoca M5al. J Bacteriol 181 : 7274 7284.
75. Wyman, C., Rombel, I., North, A.K., Bustamante, C. Kustu, S. (1997) Unusual oligomerization required for activity of NtrC, a bacterial enhancer-binding protein. Science 275 : 1614 1616.
76. 54-dependent transcriptional activator. J Bacteriol 186 : 3499 3507.
77. Zhang, X., Chaney, M., Wigneshweraraj, S.R., Schumacher, J., Bordes, P., Cannon, W. Buck, M. (2002) Mechanochemical ATPases and transcriptional activation. Mol Microbiol 45 : 895 903.