Regulation of glutamate dehydrogenase expression in Pseudomonas putida results from its direct repression by NtrC under nitrogen-limiting conditions

Molecular Microbiology

Volumn 78, Issue 2, 2010, Pages 305-319

  Hervás, Ana B ^a   Canosa, Inés ^a   Santero, Eduardo ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLUTAMATE DEHYDROGENASE; NITROGEN; NTRC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ENZYME REPRESSION; GDHA GENE; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PSEUDOMONAS PUTIDA;

BACTERIAL PROTEINS; BINDING SITES; DNA FOOTPRINTING; GENE EXPRESSION REGULATION, BACTERIAL; GLUTAMATE DEHYDROGENASE; NITROGEN; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PSEUDOMONAS PUTIDA; RNA, BACTERIAL; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

ENTEROBACTERIACEAE; PSEUDOMONAS PUTIDA;

EID: 78649344141     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07329.x     Document Type: Article

References (57)

1. Adhya, S., Geanacopoulos, M., Lewis, D.E., Roy, S., and Aki, T. (1998) Transcription regulation by repressosome and by RNA polymerase contact. Cold Spring Harb Symp Quant Biol 63: 1-9.
2. Bender, R.A. (1991) The role of the NAC protein in the nitrogen regulation of Klebsiella aerogenes. Mol Microbiol 5: 2575-2580.
3. Best, E.A., and Bender, R.A. (1990) Cloning of the Klebsiella aerogenes nac gene, which encodes a factor required for nitrogen regulation of the histidine utilization (hut) operons in Salmonella typhimurium. J Bacteriol 172: 7043-7048.
4. Blauwkamp, T.A., and Ninfa, A.J. (2002) Nac-mediated repression of the serA promoter of Escherichia coli. Mol Microbiol 45: 351-363.
5. Brenchley, J.E., Baker, C.A., and Patil, L.G. (1975) Regulation of the ammonia assimilatory enzymes in Salmonella typhimurium. J Bacteriol 124: 182-189.
6. Camacho, E.M., and Casadesus, J. (2005) Regulation of traJ transcription in the Salmonella virulence plasmid by strandspecific DNA adenine hemimethylation. Mol Microbiol 57: 1700-1718.
7. Camarena, L., Poggio, S., Garcia, N., and Osorio, A. (1998) Transcriptional repression of gdhA in Escherichia coli is mediated by the Nac protein. FEMS Microbiol Lett 167: 51-56.
8. Collins, C.M., Gutman, D.M., and Laman, H. (1993) Identification of a nitrogen-regulated promoter controlling expression of Klebsiella pneumoniae urease genes. Mol Microbiol 8: 187-198.
9. Desnoues, N., Lin, M., Guo, X., Ma, L., Carreno-Lopez, R., and Elmerich, C. (2003) Nitrogen fixation genetics and regulation in a Pseudomonas stutzeri strain associated with rice. Microbiology 149: 2251-2262.
10. Dixon, R. (1984) Tandem promoters determine regulation of the Klebsiella pneumoniae glutamine synthetase (glnA) gene. Nucleic Acids Res 12: 7811-7830.
11. Dixon, R., and Kahn, D. (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2: 621-631.
12. Dominguez-Cuevas, P., and Marqués, S. (2004) Compiling sigma 70- dependent promoters. In Pseudomonas. Ramos, J.L. (ed.). New York: Plenum Publisher, pp. 345-364.
13. Elliott, T., and Geiduschek, E.P. (1984) Defining a bacteriophage T4 late promoter: absence of a "-35" region. Cell 36: 211-219.
14. Espinosa-Urgel, M., Salido, A., and Ramos, J.L. (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182: 2363- 2369.
15. Feng, J., Goss, T.J., Bender, R.A., and Ninfa, A.J. (1995) Activation of transcription initiation from the nac promoter of Klebsiella aerogenes. J Bacteriol 177: 5523-5534.
16. Figurski, D.H., and 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.
17. Forchhammer, K. (2008) P(II) signal transducers: novel functional and structural insights. Trends Microbiol 16: 65-72.
18. Franklin, F.C., Bagdasarian, M., Bagdasarian, M.M., and 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.
19. Frisch, R.L., and Bender, R.A. (2010) An Expanded role for the nitrogen assimilation control protein (NAC) in the response of Klebsiella pneumoniae to nitrogen stress. J Bacteriol doi:10.1128/JB.00931-09.
20. Garcia-Gonzalez, V., Govantes, F., Porrua, O., and Santero, E. (2005) Regulation of the Pseudomonas sp. strain ADP cyanuric acid degradation operon. J Bacteriol 187: 155- 167.
21. Goss, T.J., Perez-Matos, A., and Bender, R.A. (2001) Roles of glutamate synthase, gltBD, and gltF in nitrogen metabolism of Escherichia coli and Klebsiella aerogenes. J Bacteriol 183: 6607-6619.
22. Goss, T.J., Janes, B.K., and Bender, R.A. (2002) Repression of glutamate dehydrogenase formation in Klebsiella aerogenes requires two binding sites for the nitrogen assimilation control protein, NAC. J Bacteriol 184: 6966-6975.
23. Govantes, F., Molina-Lopez, J.A., and Santero, E. (1996) Mechanism of coordinated synthesis of the antagonistic regulatory proteins NifL and NifA of Klebsiella pneumoniae. J Bacteriol 178: 6817-6823.
24. Govantes, F., Albrecht, J.A., and Gunsalus, R.P. (2000) Oxygen regulation of the Escherichia coli cytochrome d oxidase (cydAB) operon: roles of multiple promoters and the Fnr-1 and Fnr-2 binding sites. Mol Microbiol 37: 1456- 1469.
25. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
26. Harrod, A.C., Yang, X., Junker, M., and Reitzer, L. (2004) Evidence for a second interaction between the regulatory amino-terminal and central output domains of the response regulator NtrC (nitrogen regulator I) in Escherichia coli. J Biol Chem 279: 2350-2359.
27. Helling, R.B. (1994) Why does Escherichia coli have two primary pathways for synthesis of glutamate? J Bacteriol 176: 4664-4668.
28. Helling, R.B. (1998) Pathway choice in glutamate synthesis in Escherichia coli. J Bacteriol 180: 4571-4575.
29. Hervas, A.B., Canosa, I., and Santero, E. (2008) Transcriptome analysis of Pseudomonas putida in response to nitrogen availability. J Bacteriol 190: 416-420.
30. Hervas, A.B., Canosa, I., Little, R., Dixon, R., and Santero, E. (2009) NtrC-dependent regulatory network for nitrogen assimilation in Pseudomonas putida. J Bacteriol 191: 6123-6135.
31. Inoue, H., Nojima, H., and Okayama, H. (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96: 23-28.
32. Kohler, T., Harayama, S., Ramos, J.L., and Timmis, K.N. (1989) Involvement of Pseudomonas putida RpoN sigma factor in regulation of various metabolic functions. J Bacteriol 171: 4326-4333.
33. Kouzuma, A., Endoh, T., Omori, T., Nojiri, H., Yamane, H., and Habe, H. (2008) Transcription factors CysB and SfnR constitute the hierarchical regulatory system for the sulfate starvation response in Pseudomonas putida. J Bacteriol 190: 4521-4531.
34. Leigh, J.A., and Dodsworth, J.A. (2007) Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 61: 349-377.
35. MacFarlane, S.A., and Merrick, M. (1985) The nucleotide sequence of the nitrogen regulation gene ntrB and the glnA-ntrBC intergenic region of Klebsiella pneumoniae. Nucleic Acids Res 13: 7591-7606.
36. Mandelbaum, R.T., Wackett, L.P., and Allan, D.L. (1993) Mineralization of the s-triazine ring of atrazine by stable bacterial mixed cultures. Appl Environ Microbiol 59: 1695- 1701.
37. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual. Cold Spring harbor, NY: Cold Spring Harbor Laboratory Press.
38. Oehler, S., Eismann, E.R., Kramer, H., and Muller-Hill, B. (1990) The three operators of the lac operon cooperate in repression. EMBO J 9: 973-979.
39. Poggio, S., Domeinzain, C., Osorio, A., and Camarena, L. (2002) The nitrogen assimilation control (Nac) protein represses asnC and asnA transcription in Escherichia coli. FEMS Microbiol Lett 206: 151-156.
40. Porrua, O., Garcia-Jaramillo, M., Santero, E., and 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.
41. Porrua, O., Garcia-Gonzalez, V., Santero, E., Shingler, V., and Govantes, F. (2009) Activation and repression of a sigmaN-dependent promoter naturally lacking upstream activation sequences. Mol Microbiol 73: 419-433.
42. Porter, S.C., North, A.K., Wedel, A.B., and Kustu, S. (1993) Oligomerization of NTRC at the glnA enhancer is required for transcriptional activation. Genes Dev 7: 2258-2273.
43. Reitzer, L. (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57: 155-176.
44. Reitzer, L. (2004) Ammonia assimilation and the biosynthesis of glutamine, glutamate, aspartate, asparagine, L-alanine and D-alanine. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC: American Society for Microbiology, pp. 391-407.
45. Reitzer, L.J., and Magasanik, B. (1985) Expression of glnA in Escherichia coli is regulated at tandem promoters. Proc Natl Acad Sci USA 82: 1979-1983.
46. Riba, L., Becerril, B., Servin-Gonzalez, L., Valle, F., and Bolivar, F. (1988) Identification of a functional promoter for the Escherichia coli gdhA gene and its regulation. Gene 71: 233-246.
47. Rojo, F. (2001) Mechanisms of transcriptional repression. Curr Opin Microbiol 4: 145-151.
48. Rosario, C.J., and Bender, R.A. (2005) Importance of tetramer formation by the nitrogen assimilation control protein for strong repression of glutamate dehydrogenase formation in Klebsiella pneumoniae. J Bacteriol 187: 8291- 8299.
49. Sambrook, J., Fritsch, E.F., and Maniatis, T. (2000) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
50. Schwab, S., Souza, E.M., Yates, M.G., Persuhn, D.C., Steffens, M.B., Chubatsu, L.S., et al. (2007) The glnAntrBC operon of Herbaspirillum seropedicae is transcribed by two oppositely regulated promoters upstream of glnA. Can J Microbiol 53: 100-105.
51. Schwacha, A., and Bender, R.A. (1993) The nac (nitrogen assimilation control) gene from Klebsiella aerogenes. J Bacteriol 175: 2107-2115.
52. Totten, P.A., Lara, J.C., and Lory, S. (1990) The rpoN gene product of Pseudomonas aeruginosa is required for expression of diverse genes, including the flagellin gene. J Bacteriol 172: 389-396.
53. Wigneshweraraj, S., Bose, D., Burrows, P.C., Joly, N., Schumacher, J., Rappas, M., et al. (2008) Modus operandi of the bacterial RNA polymerase containing the sigma54 promoter-specificity factor. Mol Microbiol 68: 538-546.
54. Yang, X.F., Ji, Y., Schneider, B.L., and Reitzer, L. (2004) Phosphorylation-independent dimer-dimer interactions by the enhancer-binding activator NtrC of Escherichia coli: a third function for the C-terminal domain. J Biol Chem 279: 36708-36714.
55. Yuste, L., Hervas, A.B., Canosa, I., Tobes, R., Jimenez, J.I., Nogales, J., et al. (2006) Growth phase-dependent expression of the Pseudomonas putida KT2440 transcriptional machinery analysed with a genome-wide DNA microarray. Environ Microbiol 8: 165-177.
56. Zhang, X., Chaney, M., Wigneshweraraj, S.R., Schumacher, J., Bordes, P., Cannon, W., and Buck, M. (2002) Mechanochemical ATPases and transcriptional activation. Mol Microbiol 45: 895-903.
57. Zimmer, D.P., Soupene, E., Lee, H.L., Wendisch, V.F., Khodursky, A.B., Peter, B.J., et al. (2000) Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation. Proc Natl Acad Sci USA 97: 14674-14679.