Characterization of the norCBQD genes, encoding nitric oxide reductase, in the nitrogen fixing bacterium Bradyrhizobium japonicum

Microbiology

Volumn 148, Issue 11, 2002, Pages 3553-3560

  Mesa, Socorro ^a   Velasco, Leonardo ^b   Manzanera, Maximino E ^c   Delgado, María J ^a   Bedmar, Eulogio J ^a  

^a Estacion Exper del Zaidin   (Spain)

^b Centro Invest Foramcion Horticola   (Spain)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Denitrification; Nitrate; Nitric oxide reduction; Regulation; Rhizobium; Transcription

Indexed keywords

ADENOSINE TRIPHOSPHATE BINDING PROTEIN; BETA GALACTOSIDASE; BINDING PROTEIN; CYTOCHROME B; CYTOCHROME C; GENE PRODUCT; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE PROTEIN; NITRATE; NITRIC OXIDE; NITRIC OXIDE REDUCTASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FIXK2; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIUM CULTURE; BACTERIUM ISOLATION; BACTERIUM MUTANT; BRADYRHIZOBIUM JAPONICUM; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME SUBUNIT; GENE FUNCTION; GENE FUSION; GENETIC CODE; GENETIC TRANSCRIPTION; MUTATIONAL ANALYSIS; NITROGEN FIXATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN MOTIF; REPORTER GENE; REVIEW; SEQUENCE HOMOLOGY; STRUCTURAL GENE; WILD TYPE;

BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM JAPONICUM; NEGIBACTERIA; PROKARYOTA; RHIZOBIUM; TRIXIS;

EID: 0041347813     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-148-11-3553     Document Type: Review

References (57)

1. Amarger, N. (2001). Rhizobia in the field. Adv Agron 73, 109-168.
2. Anthamatten, D. & Hennecke, H. (1991). The regulatory status of the fixL- and fixJ-like genes in Bradyrhizobium japonicum may be different from that in Rhizobium meliloti. Mol Gen Genet 225, 38-48.
3. Arai, H., Igarashi, Y. & Kodama, T. (1995). The structural genes for nitric oxide reductase from Pseudomonas aeruginosa. Biochim Biophys Acta 1261, 279-284.
4. Arai, H., Kodama, T. & Igarashi, Y. (1997). Cascade regulation of the two CRP/FNR-related transcriptional regulators (ANR and DNR) and the denitrification enzymes in Pseudomonas aeruginosa. Mol Microbiol 25, 1141-1148.
5. Arai, H., Kodama, T. & Higarashi, Y. (1999). Effect of nitrogen oxides on expression of the nir and nor genes for denitrification in Pseudomonas aeruginosa. FEMS Microbiol Lett 170, 19-24.
6. Baker, S. C., Ferguson, S. J., Ludwig, B., Page, M. D., Richter, O.-M. H. & van Spanning, R. J. M. (1998). Molecular genetics of the genus Paracoccus: metabolically versatile bacteria with bioenergetic flexibility. Microbiol Mol Biol Rev 62, 1046-1078.
7. Bartnikas, T. B., Tosques, I. E., Laratta, W. P., Shi, J. & Shapleigh, J. P. (1997). Characterization of the nitric oxide reductase-encoding region in Rhodobacter sphaeroides 2.4.3. J Bacteriol 179, 3534-3540.
8. Bates, J. N., Baker, M. T., Guerra, R., Jr & Harrison, D. G. (1991). Nitric oxide generation from nitroprusside by vascular tissue: evidence that reduction of the nitroprusside anion and cyanide loss are required. Biochem Pharmacol 42(Suppl), 5157-5165.
9. Bedzyk, L., Wang, T. & Ye, R. W. (1999). The periplasmic nitrate reductase in Pseudomonas sp. strain G-179 catalyzes the first step of denitrification. J Bacteriol 181, 2802-2806.
10. Bott, M., Ritz, D. & Hennecke, H. (1991). The Bradyrhizobium japonicum cycM gene encodes a membrane-anchored homolog of mitochondrial cytochrome c. J Bacteriol 173, 6766-6772.
11. Büsch, A., Friedrich, B. & Cramm, R. (2002). Characterization of the norB gene, encoding nitric oxide reductase, in the nondenitrifying cyanobacterium Synechocystis sp. strain PCC6803. Appl Environ Microbiol 68, 668-672.
12. Cramm, R., Siddiqui, R. A. & Friedrich, B. (1997). Two isofunctional nitric oxide reductases in Alcaligenes eutrophus H16. J Bacteriol 179, 6769-6777.
13. Cramm, R., Pohlman, A. & Friedrich, B. (1999). Purification and characterization of the single-component nitric oxide reductase from Ralstonia eutropha H16. FEBS Lett 460, 6-10.
14. de Boer, A. P., van der Oost, J., Reijnders, W. N. H., Westerhoff, V., Stouthamer, A. H. & van Spanning, R. J. M. (1996). Mutational analysis of the nor gene cluster which encodes nitric-oxide reductase from Paracoccus denitrificans. Eur J Biochem 242, 592-600.
15. 2 protein is involved in regulation of symbiotic hydrogenase expression in Bradyrhizobium japonicum. J Bacteriol 180, 3253-3256.
16. Fischer, H. M. (1994). Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58, 352-386.
17. Fischer, H. M., Velasco, L., Delgado, M. J., Bedmar, E. J., Schären, S., Zingg, D., Göttfert, M. & Hennecke, H. (2001). One of two hemN genes in Bradyrhizobium japonicum is functional during anaerobic growth and in symbiosis. J Bacteriol 183, 1300-1311.
18. Gilles-Gonzalez, M. A., Gonzalez, G. & Perutz, M. F. (1995). Kinase activity of oxygen sensor FixL depends on the spin state of its heme iron. Biochemistry 34, 232-236.
19. Hendriks, J., Oubrie, A., Castresana, J., Urbani, A., Gemeinhardt, S. & Saraste, M. (2000). Nitric oxide reductase in bacteria. Biochim Biophys Acta 1459, 266-273.
20. Hutchings, M. I. & Spiro, S. (2000). The nitric oxide regulated nor promoter of Paracocus denitrificans. Microbiology 146, 2635-2641.
21. Jüngst, A. & Zumft, W. G. (1992). Interdependence of respiratory NO reduction and nitrite reduction revealed by mutagenesis of nirQ, a novel gene in the denitrification gene cluster of Pseudomonas stutzeri. FEBS Lett 314, 308-314.
22. Kovach, M. E., Phillips, R. W., Elzer, P. H., Roop, R. M., 2nd & Peterson, K. M. (1994). pBBR1MCS: a broad-host-range cloning vector. BioTechniques 16, 800-802.
23. Kukimoto, M., Nishiyama, M., Tanokura, M. & Horinouchi, S. (2000). Gene organization for nitric oxide reduction in Alcaligenes faecalis S-6. Biosci Biotechnol Biochem 64, 852-857.
24. Kündig, C., Hennecke, H. & Göttfert, M. (1993). Correlated and physical map of the Bradyrhizobium japonicum 110 genome. J Bacteriol 175, 613-622.
25. Kwiatkowski, A. & Shapleigh, J. P. (1996). Requirement of nitric oxide for induction of genes whose products are involved in nitric oxide metabolism in Rhodobacter sphaeroides 2.4.3. J Biol Chem 271, 24382-24388.
26. Miller, J. H. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
27. 2, a crucial distributor in the FixLJ-dependent regulatory cascade for control of genes inducible by low oxygen. J Bacteriol 180, 5251-5255.
28. Nienaber, A., Huber, A., Göttfert, M., Hennecke, H. & Fischer, H. M. (2000). Three new NifA-regulated genes in the Bradyrhizobium japonicum symbiotic gene region discovered by competitive DNA-RNA hybridization. J Bacteriol 182, 1472-1480.
29. O'Hara, G. W. & Daniel, R. (1985). Rhizobial denitrification: a review. Soil Biol Biochem 17, 1-9.
30. Preisig, O., Anthamatten, D. & Hennecke, H. (1993). Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc Natl Acad Sci USA 90, 3309-3313.
31. 3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 178, 1532-1538.
32. Regensburger, B. & Hennecke, H. (1983). RNA polymerase from Rhizobium japonicum. Arch Microbiol 135, 103-109.
33. Richardson, D. J. & Watmough, N. J. (1999). Inorganic nitrogen metabolism in bacteria. Curr Opin Chem Biol 3, 297-219.
34. Rodgers, K. R., Lukat-Rodgers, G. S. & Tang, L. (2000). Nitrosyl adducts of FixL as probes of heme environment. J Biol Inorg Chem 5, 642-654.
35. Sakurai, N. & Sakurai, T. (1997). Isolation and characterization of nitric oxide reductase from Paracoccus halodenitrificans. Biochemistry 36, 13809-13815.
36. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
37. Simon, R., Priefer, U. & Pühler, A. (1983). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1, 784-791.
38. Spaink, H. P., Okker, H. R. J., Wijffelman, C. A., Pees, E. & Lugtenberg, B. J. J. (1987). Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol 9, 27-39.
39. Spiro, S. (1994). The FNR family of transcriptional regulators. Antonie Leeuwenhoek 66, 23-36.
40. 1 complex in Bradyrhizobium japonicum and its requirement for effective root nodule symbiosis. Cell 57, 683-697.
41. Tosques, I. E., Shi, J. & Shapleigh, J. P. (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.
42. Tuckerman, J. R., Gonzalez, G. & Gilles-Gonzalez, M. A. (2001). Complexation precedes phosphorylation for two-component regulatory system FixL/FixJ of Sinorhizobium meliloti. J Mol Biol 308, 449-455.
43. Vairinhos, F., Wallace, W. & Nicholas, D. J. D. (1989). Simultaneous assimilation and denitrification of nitrate by Bradyrhizobium japonicum. J Gen Microbiol 135, 189-193.
44. van Spanning, R. J. M., de Boer, A. P., Reijnders, W. N., Spiro, S., Westerhoff, H. V., Stouthamer, A. H. & van der Oost, J. (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.
45. van Spanning, R. J. M., Houben, E., Reijnders, W. N. M., Spiro, S., Westerhoff, A., Stouthamer, H. V. & Saunders, N. (1999). Nitric oxide is a signal for NNR-mediated transcription activation in Paracoccus denitrificans. J Bacteriol 181, 4129-4132.
46. Vargas, C., McEwan, A. G. & Downie, J. A. (1993). Detection of c-type cytochromes using enhanced chemiluminiscence. Anal Biochem 209, 323-326.
47. Velasco, L., Mesa, S., Delgado, M. J. & Bedmar, E. J. (2001). Characterization of the nirK gene encoding the respiratory Cu-containing nitrite redutase of Bradyrhizobium japonicum. Biochim Biophys Acta 1521, 130-134.
48. Vincent, J. M. (1974). Root-nodule symbioses with Rhizobium. In The Biology of Nitrogen Fixation, pp. 265-341. Edited by A. Quispel. New York: Elsevier.
49. Vollack, K.-U. & Zumft, W. G. (2001). Nitric oxide signaling and transcriptional control of denitrification genes in Pseudomonas stutzeri. J Bacteriol 183, 2516-2526.
50. Vollack, K.-U., Härtig, E., Körner, H. & Zumft, W. G. (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.
51. Walker, J. E., Saraste, M., Runswick, M. J. & Gay, N. J. (1982). Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1, 945-951.
52. Watmough, N. J., Butland, G., Cheesman, M. R., Moir, J. W. B., Richardson, D. J. & Spiro, S. (1999). Nitric oxide in bacteria synthesis and consumption. Biochim Biophys Acta 1411, 456-474.
53. Wing, H. J., Williams, S. M. & Busby, S. J. (1995). Spacing requirements for transcription activation by Escherichia coli FNR protein. J Bacteriol 177, 6704-6710.
54. Yanisch-Perron, C., Vieira, J. & Messing, J. (1985). Improved M13 phage cloning vectors and strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119.
55. Yoshida, M. & Amano, T. (1995). A common topology of proteins catalyzing ATP-triggered reactions. FEBS Lett 359, 1-5.
56. Zumft, W. G. (1997). Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 4, 533-616.
57. Zumft, W. G., Braun, C. & Cuypers, H. (1994). Nitric oxide reductase from Pseudomonas stutzeri: primary structure and gene organization of a novel bacterial cytochrome bc complex. Eur J Biochem 219, 481-490.