A DNA region recognized by the nitric oxide-responsive transcriptional activator NorR is conserved in β and γ-proteobacteria

Journal of Bacteriology

Volumn 186, Issue 23, 2004, Pages 7980-7987

  Büsch, Andrea ^a   Pohlmann, Anne ^a   Friedrich, Bärbel ^a   Cramm, Rainer ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DEOXYRIBONUCLEASE I; NITRIC OXIDE; NITRIC OXIDE REDUCTASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NORR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; DNA FOOTPRINTING; GENE LOCUS; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WAUTERSIA EUTROPHA;

BASE SEQUENCE; BETAPROTEOBACTERIA; BINDING SITES; CONSERVED SEQUENCE; DNA, BACTERIAL; GAMMAPROTEOBACTERIA; GENES, REGULATOR; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; PROMOTER REGIONS (GENETICS); TRANS-ACTIVATORS;

BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA; NEGIBACTERIA; PROKARYOTA; PROTEOBACTERIA; RALSTONIA; WAUTERSIA EUTROPHA;

EID: 9244233838     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.23.7980-7987.2004     Document Type: Article

References (60)

1. Anjum, M. F., T. M. Stevanin, R. C. Read, and J. W. Moir. 2002. Nitric oxide metabolism in Neisseria meningitidis. J. Bacteriol. 184:2987-2993.
2. Arai, H., T. Kodama, and Y. Igarashi. 1999. Effect of nitrogen oxides on expression of the nir and nor genes for denitrification in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 170:19-24.
3. Aravind, L., and C. P. Ponting. 1997. The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem. Sci. 22:458-459.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1998. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
5. Beaumont, H. J., B. van Schooten, S. I. Lens, H. V. Westerhoff, and R. J. van Spanning. 2004. Nitrosomonas europaea expresses a nitric oxide reductase during nitrification. J. Bacteriol. 186:4417-4421.
6. Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
7. Büsch, A., B. Friedrich, and R. Cramm. 2002. Characterization of the norB gene, encoding nitric oxide reductase, in the nondenitrifying cyanobacterium Synechocystis sp. strain PCC6803. Appl. Environ. Microbiol. 68:668-672.
8. Chen, B., and A. E. Przybyla. 1994. An efficient site-directed mutagenesis method based on PCR. BioTechniques 17:657-659.
9. Corker, H., and R. K. Poole. 2003. Nitric oxide formation by Escherichia coli. Dependence on nitrite reductase, the NO-sensing regulator Fnr, and flavohemoglobin Hmp. J. Biol. Chem. 278:31584-31592.
10. Cramm, R., R. A. Siddiqui, and B. Friedrich. 1997. Two isofunctional nitric oxide reductases in Alcaligenes eutrophus H16. J. Bacteriol. 179:6769-6777.
11. Cramm, R., A. Pohlmann, and B. Friedrich. 1999. Purification and characterization of the single-component nitric oxide reductase from Ralstonia eutropha H16. FEBS Lett. 460:6-10.
12. Crawford, M. J., and D. E. Goldberg. 1998. Regulation of the Salmonella typhimurium flavohemoglobin gene. A new pathway for bacterial gene expression in response to nitric oxide. J. Biol. Chem. 273:34028-34032.
13. Demple, B. 1999. Radical ideas: genetic responses to oxidative stress. Clin. Exp. Pharmacol. Physiol. 26:64-68.
14. Deng, W., S. R. Liou, G. Plunkett III, G. F. Mayhew, D. J. Rose, V. Burland, V. Kodoyianni, D. C. Schwartz, and F. R. Blattner. 2003. Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J. Bacteriol. 185:2330-2337.
15. 2:NO oxidoreductase from the hyperthermophilic archaeon Pyrobaculum aerophilum. J. Biol. Chem. 278:35861-35868.
16. Ding, H., and B. Demple. 2000. Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator. Proc. Natl. Acad. Sci. USA 97:5146-5150.
17. Gardner, A. M., R. A. Helmick, and P. R. Gardner. 2002. Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli. J. Biol. Chem. 277:8172-8177.
18. Gardner, A. M., C. R. Gessner, and P. R. Gardner. 2003. Regulation of the nitric oxide reduction operon (norRVW) in Escherichia coli. Role of NorR and sigma54 in the nitric oxide stress response. J. Biol. Chem. 278:10081-10086.
19. Gardner, P. R., A. M. Gardner, L. A. Martin, and A. L. Salzman. 1998. Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proc. Natl. Acad. Sci. USA 95:10378-10383.
20. Gomes, C. M., A. Giuffre, E. Forte, J. B. Vicente, L. M. Saraiva, M. Brunori, and M. Teixeira. 2002. A novel type of nitric-oxide reductase. Escherichia coli flavorubredoxin. J. Biol. Chem. 277:25273-25276.
21. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
22. Hausladen, A., C. T. Privalle, T. Keng, J. DeAngelo, and J. S. Stamler. 1996. Nitrosative stress: activation of the transcription factor OxyR. Cell 86:719-729.
23. Heidelberg, J. F., J. A. Eisen, W. C. Nelson, R. A. Clayton, M. L. Gwinn, R. J. Dodson, D. H. Haft, E. K. Hickey, J. D. Peterson, L. Umayam, S. R. Gill, K. E. Nelson, T. D. Read, H. Tettelin, D. Richardson, M. D. Ermolaeva, J. Vamathevan, S. Bass, H. Qin, I. Dragoi, P. Sellers, L. McDonald, T. Utterback, R. D. Fleishmann, W. C. Nierman, and O. White. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406:477-483.
24. Householder, T. C., E. M. Fozo, J. A. Cardinale, and V. L. Clark. 2000. Gonococcal nitric oxide reductase is encoded by a single gene, norB, which is required for anaerobic growth and is induced by nitric oxide. Infect. Immun. 68:5241-5246.
25. Huffman, J. L., and R. G. Brennan. 2002. Prokaryotic transcription regulators: more than just the helix-turn-helix motif. Curr. Opin. Struct. Biol. 12:98-106.
26. Hutchings, M. I., N. Mandhana, and S. Spiro. 2002. The NorR protein of Escherichia coli activates expression of the flavorubredoxin gene norV in response to reactive nitrogen species. J. Bacteriol. 184:4640-4643.
27. Kim, C. C., D. Monack, and S. Falkow. 2003. Modulation of virulence by two acidified nitrite-responsive loci of Salmonella enterica serovar Typhimurium. Infect. Immun. 71:3196-3205.
28. Kim, Y. R., S. E. Lee, C. M. Kim, S. Y. Kim, E. K. Shin, D. H. Shin., S. S. Chung, H. E. Choy, A. Progulske-Fox, J. D. Hillman, M. Handfield, and J. H. Rhee. 2003. Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect. Immun. 71:5461-5471.
29. Kwiatkowski, A. V., W. P. Laratta, A. Toffanin, and J. P. Shapleigh. 1997. Analysis of the role of the nnrR gene product in the response of Rhodobacter sphaeroides 2.4.1 to exogenous nitric oxide. J. Bacteriol. 179:5618-5620.
30. Lowry, D. R., N. J. Rosebroug, A. L. Fair, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
31. McClelland, M., K. E. Sanderson, J. Spieth, S. W. Clifton, P. Latreille, L. Courtney, S. Porwollik, J. Ali, M. Dante, F. Du, S. Hou, D. Layman, S. Leonard, C. Nguyen, K. Scott, A. Holmes, N. Grewal, E. Mulvaney, E. Ryan, H. Sun, L. Florea, W. Miller, T. Stoneking, M. Nhan, R. Waterston, and R. K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852-856.
32. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
33. 54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains. J. Bacteriol. 175:6067-6074.
34. Mukhopadhyay, P., M. Zheng, L. A. Bedzyk, R. A. LaRossa, and G. Storz. 2004. Prominent roles of the NorR and Fur regulators in the Escherichia coli transcriptional response to reactive nitrogen species. Proc. Natl. Acad. Sci. USA 101:745-750.
35. Nakano, M. M. 2002. Induction of ResDE-dependent gene expression in Bacillus subtilis in response to nitric oxide and nitrosative stress. J. Bacteriol. 184:1783-1787.
36. North, A. K., K. E. Klose, K. M. Stedman, and S. Kustu. 1993. Prokaryotic enhancer-binding proteins reflect eukaryote-like modularity: the puzzle of nitrogen regulatory protein C. J. Bacteriol. 175:4267-4273.
37. Pohlmann, A., R. Cramm, K. Schmelz, and B. Friedrich. 2000. A novel NO-responding regulator controls the reduction of nitric oxide in Ralstonia eutropha. Mol. Microbiol. 38:626-638.
38. Poole, R. K., and M. N. Hughes. 2000. New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 36:775-783.
39. Ray, P., K. J. Smith, R. A. Parslow, R. Dixon, and E. I. Hyde. 2002. Secondary structure and DNA binding by the C-terminal domain of the transcriptional activator NifA from Klebsiella pneumoniae. Nucleic Acids Res. 30:3972-3980.
40. Rice, P. A. 1997. Making DNA do a U-turn: IHF and related proteins. Curr. Opin. Struct. Biol. 7:86-93.
41. Salanoubat M., S. Genin, F. Artiguenave, J. Gouzy, S. Mangenot, M. Arlat, A. Billault, P. Brottier, J. C. Camus, L. Cattolico, M. Chandler, N. Choisne, C. Claudel-Renard, S. Cunnac, N. Demange, C. Gaspin, M. Lavie, A. Moisan, C. Robert, W. Saurin, T. Schiex, P. Siguier, P. Thebault, M. Whalen, P. Wincker, M. Levy, J. Weissenbach, and C. A. Boucher. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497-502.
42. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
43. Schlegel, H. G., H. Kaltwasser, and G. Gottschalk. 1961. Ein Submersverfahren zur Kultur wasserstoffoxidierender Bakterien: Wachstumsphysiologische Untersuchungen. Arch. Mikrobiol. 38:315-324.
44. Schmidt, I., P. J. M. Steenbakkers, H. J. M. op den Camp, K. Schmidt, and M. S. M. Jetten. 2004. Physiologic and proteomic evidence for a role of nitric oxide in biofilm formation by Nitrosomonas europaea and other ammonia oxidizers. J. Bacteriol. 186:2781-2788.
45. Schwartz, E., U. Gerischer, and B. Friedrich. 1998. Transcriptional regulation of Alcaligenes eutrophus hydrogenase genes. J. Bacteriol. 180:3197-3204.
46. Schwartz, E., and B. Friedrich. 2001. A physical map of the megaplasmid pHG1, one of three genomic replicons in Ralstonia eutropha H16. FEMS Microbiol. Lett. 201:213-219.
47. 2-based lithoautotrophy and anaerobiosis. J. Mol. Biol. 332:369-383.
48. Shingler, V. 1996. Signal sensing by sigma 54-dependent regulators: derepression as a control mechanism. Mol. Microbiol. 19:409-416.
49. Shingler, V. 2003. Integrated regulation to aromatic compounds: from signal sensing to attractive behaviour. Environ. Microbiol. 5:1226-1241.
50. Simon, R., U. Priefer, and A. Pühler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Bio/Technology 1:784-791.
51. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. Wong, Z. Wu, I. T. Paulsen, J. Reizer, M. H. Saier, R. E. Hancock, S. Lory, and M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406:959-964.
52. 54-dependent transcriptional activators. J. Bacteriol. 185:1757-1767.
53. Studier, F. W., and B. A. Moffatt. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130.
54. Tosques, I. E., J. Shi, and J. P. Shapleigh. 1996. Cloning and characterization of nnrR, whose product is required for the expression of proteins involved in nitric oxide metabolism in Rhodobacter sphaeroides 2.4.3. J. Bacteriol. 178:4958-4964.
55. Van Spanning, R. J., A. P. De Boer, W. N. Reijnders, S. Spiro, H. V. Westerhoff, A. H. Stouthamer, and J. Van der Oost. 1995. Nitrite and nitric oxide reduction in Paracoccus denitrificans is under the control of NNR, a regulatory protein that belongs to the FNR family of transcriptional activators. FEBS Lett. 360:151-154.
56. Van Spanning, R. J., E. Houben, W. N. Reijnders, S. Spiro, H. V. Westerhoff, and N. Saunders. 1999. Nitric oxide is a signal for NNR-mediated transcription activation in Paracoccus denitrificans. J. Bacteriol. 181:4129-4132.
57. Vollack, K. U., E. Härtig, H. Körner, and W. G. Zumft. 1999. Multiple transcription factors of the FNR family in denitrifying Pseudomonas stutzeri: characterization of four fnr-like genes, regulatory responses and cognate metabolic processes. Mol. Microbiol. 31:1681-1694.
58. Vollack, K. U., and W. G. Zumft. 2001. Nitric oxide signaling and transcriptional control of denitrification genes in Pseudomonas stutzeri. J. Bacteriol. 183:2516-2526.
59. Wintjens, R., and M. Rooman. 1996. Structural classification of HTH DNA-binding domains and protein-DNA interaction modes. J. Mol. Biol. 262:294-313.
60. Zimmer, D., E. Schwartz, A. Tran-Betcke, P. Gewinner, and B. Friedrich. 1995. Temperature tolerance of hydrogenase expression in Alcaligenes eutrophus is conferred by a single amino acid exchange in the transcriptional activator HoxA. J. Bacteriol. 177:2373-2380.