Characterization of a novel copper-haem c dissimilatory nitrite reductase from Ralstonia pickettii

Biochemical Journal

Volumn 444, Issue 2, 2012, Pages 219-226

  Han, Cong ^a   Wright, Gareth S A ^a   Fisher, Karl ^b   Rigby, Stephen E J ^b   Eady, Robert R ^a   Hasnain, S Samar ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Autoinduction; c type haem; Gel permeation chromatography; Nitrite reductase (NiR); Ralstonia pickettii; Small angle X ray scattering (SAXS)

Indexed keywords

COPPER ION; NITRITE REDUCTASE;

ABSORPTION SPECTROSCOPY; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ESCHERICHIA COLI; GEL FILTRATION; GEL PERMEATION CHROMATOGRAPHY; METAL BINDING; MOLECULAR CLONING; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PURIFICATION; RALSTONIA PICKETTII; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; COPPER; HEME; MOLECULAR SEQUENCE DATA; NITRITE REDUCTASES; RALSTONIA PICKETTII; SCATTERING, SMALL ANGLE; X-RAY DIFFRACTION;

ACHROMOBACTER XYLOSOXIDANS; ESCHERICHIA COLI; RALSTONIA PICKETTII;

EID: 84860880998     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111623     Document Type: Article

References (43)

1. Zumft, W. G. (1997) Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533-616
2. Van Spanning, R. J. M., Richardson, D. J. and Ferguson, S. J. (2007) Introduction to the biochemistry and molecular biology of denitrification. In Biology of the Nitrogen Cycle (Bothe, H., Ferguson, S. and Newton, W. E., eds), pp. 3-20, Elsevier, Amsterdam
3. Shoun, H. and Tanimoto, T. (1991) Denitrification by the fungus Fusarium oxysporum and involvement of cytochrome P-450 in the respiratory nitrite reduction. J. Biol. Chem. 266, 11078-11082 (Pubitemid 21906914)
4. Godden, J. W., Turley, S., Teller, D. C., Adman, E. T., Liu, M. Y., Payne, W. J. and LeGall, J. (1991) The 2.3 angstrom X-ray structure of nitrite reductase from Achromobacter cycloclastes. Science 253, 438-442 (Pubitemid 21917172)
5. 2 - bound and with type II copper depleted. J. Biol. Chem. 270, 27458-27474
6. Kukimoto, M., Nishiyama, M., Murphy, M. E., Turley, S., Adman, E. T., Horinouchi, S. and Beppu, T. (1994) X-ray structure and site-directed mutagenesis of a nitrite reductase from Alcaligenes faecalis S-6: roles of two copper atoms in nitrite reduction. Biochemistry 33, 5246-5252
7. Murphy, M. E., Turley, S. and Adman, E. T. (1997) Structure of nitrite bound to copper-containing nitrite reductase from Alcaligenes faecalis. Mechanistic implications. J. Biol. Chem. 272, 28455-28460 (Pubitemid 27517793)
8. Inoue, T., Gotowda, M., Deligeer, Kataoka, K., Yamaguchi, K., Suzuki, S., Watanabe, H., Gohow, M. and Kai, Y. (1998) Type 1 Cu structure of blue nitrite reductase from Alcaligenes xylosoxidans GIFU 1051 at 2.05 Å resolution: comparison of blue and green nitrite reductases. J. Biochem. 124, 876-879 (Pubitemid 28544894)
9. Dodd, F. E., Van Beeumen, J., Eady, R. R. and Hasnain, S. S. (1998) X-ray structure of a blue-copper nitrite reductase in two crystal forms. The nature of the copper sites, mode of substrate binding and recognition by redox partner. J. Mol. Biol. 282, 369-382 (Pubitemid 28418790)
10. Jacobson, F., Guo, H., Olesen, K., Okvist, M., Neutze, R. and Sjolin, L. (2005) Structures of the oxidized and reduced forms of nitrite reductase from Rhodobacter sphaeroides 2.4.3 at high pH: changes in the interactions of the type 2 copper. Acta Crystallogr. Sect. D Biol. Crystallogr. 61, 1190-1198 (Pubitemid 43961290)
11. Jacobson, F., Pistorius, A., Farkas, D., De Grip, W., Hansson, O., Sjolin, L. and Neutze, R. (2007) pH dependence of copper geometry, reduction potential, and nitrite affinity in nitrite reductase. J. Biol. Chem. 282, 6347-6355 (Pubitemid 47100846)
12. Howes, B. D., Abraham, Z. H., Lowe, D. J., Bruser, T., Eady, R. R. and Smith, B. E. (1994) EPR and electron nuclear double resonance (ENDOR) studies show nitrite binding to the type 2 copper centers of the dissimilatory nitrite reductase of Alcaligenes xylosoxidans (NCIMB 11015). Biochemistry 33, 3171-3177 (Pubitemid 24112626)
13. Prudencio, M., Eady, R. R. and Sawers, G. (1999) The blue copper-containing nitrite reductase from Alcaligenes xylosoxidans: cloning of the nirA gene and characterization of the recombinant enzyme. J. Bacteriol. 181, 2323-2329 (Pubitemid 29181551)
14. Iwasaki, H., Noji, S. and Shidara, S. (1975) Achromobacter cycloclastes nitrite reductase. The function of copper, amino acid composition, and ESR spectra. J. Biochem. 78, 355-361
15. Kakutani, T., Watanabe, H., Arima, K. and Beppu, T. (1981) Purification and properties of a copper-containing nitrite reductase from a denitrifying bacterium, Alcaligenes faecalis strain S-6. J. Biochem. 89, 453-461 (Pubitemid 11107958)
16. Olesen, K., Veselov, A., Zhao, Y., Wang, Y., Danner, B., Scholes, C. P. and Shapleigh, J. P. (1998) Spectroscopic, kinetic, and electrochemical characterization of heterologously expressed wild-type and mutant forms of copper-containing nitrite reductase from Rhodobacter sphaeroides 2.4.3. Biochemistry 37, 6086-6094 (Pubitemid 28196765)
17. LaCroix, L. B., Shadle, S. E., Wang, Y., Averill, B. A., Hedman, B., Hodgson, K. O. and Solomon, E. I. (1996) Electronic structure of the perturbed blue copper site in nitrite reductase: spectroscopic properties, bonding and implications for the entatic/rack state. J. Am. Chem. Soc. 118, 7755-7768 (Pubitemid 26285127)
18. Rinaldo, S. and Cutruzzola, F. (2007) Nitrite reductases in denitrification. In Biology of the Nitrogen Cycle (Bothe, H., Ferguson, S. and Newton, W. E., eds), pp. 37-55, Elsevier, Amsterdam
19. Deligeer, Fukunaga, R., Kataoka, K., Yamaguchi, K., Kobayashi, K., Tagawa, S. and Suzuki, S. (2002) Spectroscopic and functional characterization of Cu-containing nitrite reductase from Hyphomicrobium denitrificans A3151. J. Inorg. Biochem. 91, 132-138
20. Yamaguchi, K., Kataoka, K., Kobayashi, M., Itoh, K., Fukui, A. and Suzuki, S. (2004) Characterization of two type 1 Cu sites of Hyphomicrobium denitrificans nitrite reductase: a new class of copper-containing nitrite reductases. Biochemistry 43, 14180-14188 (Pubitemid 39485244)
21. Nojiri, M., Xie, Y., Inoue, T., Yamamoto, T., Matsumura, H., Kataoka, K., Deligeer, Yamaguchi, K., Kai, Y. and Suzuki, S. (2007) Structure and function of a hexameric copper-containing nitrite reductase. Proc. Natl. Acad. Sci. U.S.A. 104, 4315-4320 (Pubitemid 47186223)
22. Bertini, I., Cavallaro, G. and Rosato, A. (2006) Cytochrome c : occurrence and functions. Chem. Rev. 106, 90-115
23. Ishikawa, R., Nojiri, M., Yamaguchi, K. and Suzuki, S. (2009) Intermolecular electron transfer reaction of c -type heme-containing copper nitrite reductase from Pseudoalteromonas haloplanktis TAC125. J. Biol. Inorg. Chem. 14 (Suppl. 1), S107
24. Ellis, M. J., Grossmann, J. G., Eady, R. R. and Hasnain, S. S. (2007) Genomic analysis reveals widespread occurrence of new classes of copper nitrite reductases. J. Biol. Inorg. Chem. 12, 1119-1127 (Pubitemid 47594256)
25. Ryan, M. P., Pembroke, J. T. and Adley, C. C. (2007) Ralstonia pickettii in environmental biotechnology: potential and applications. J. Appl. Microbiol. 103, 754-764 (Pubitemid 47493258)
26. Arslan, E., Schulz, H., Zufferey, R., Kunzler, P. and Thony-Meyer, L. (1998) Overproduction of the Bradyrhizobium japonicum c -type cytochrome subunits of the cbb3 oxidase in Escherichia coli. Biochem. Biophys. Res. Commun. 251, 744-747 (Pubitemid 28512781)
27. Nicholas, J. D. and Nason, A. (1957) Determination of nitrate and nitrite. Methods Enzymol. 3, 981-984
28. Brenner, S., Heyes, D. J., Hay, S., Hough, M. A., Eady, R. R., Hasnain, S. S. and Scrutton, N. S. (2009) Demonstration of proton-coupled electron transfer in the copper-containing nitrite reductases. J. Biol. Chem. 284, 25973-25983
29. David, G. and P'erez, J. (2009) Combined sampler robot and high-performance liquid chromatography: a fully automated system for biological small-angle X-ray scattering experiments at the Synchrotron SOLEIL SWING beamline. J. Appl. Crystallogr. 42, 892-900
30. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. and Svergun, D. I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282
31. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
32. Grossmann, G. J. and Hasnain, S. S. (1997) X-ray scattering studies of metalloproteins in solution: a quantitative approach for studying molecular conformations, a quantitative approach for studying molecular conformations. J. Appl. Crystallogr. 30, 770-775
33. Svergun, D., Barberato, C. and Koch, M. H. J. (1995) CRYSOL: a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773 (Pubitemid 3014671)
34. Fischer, H., Oliveira Neto, M., Napolitano, H. B., Polikarpov, I. and Craievich, A. F. (2009) Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale. J. Appl. Crystallogr. 43, 101-109
35. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207-234
36. Bendtsen, J. D., Nielsen, H., von Heijne, G. and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795 (Pubitemid 38829638)
37. Gouet, P., Courcelle, E., Stuart, D. I. and Metoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (Pubitemid 29213756)
38. Zoppellaro, G., Bren, K. L., Ensign, A. A., Harbitz, E., Kaur, R., Hersleth, H. P., Ryde, U., Hederstedt, L. and Andersson, K. K. (2009) Review: studies of ferric heme proteins with highly anisotropic/highly axial low spin (S = 1/2) electron paramagnetic resonance signals with bis-histidine and histidine-methionine axial iron coordination. Biopolymers 91, 1064-1082
39. Libby, E. and Averill, B. A. (1992) Evidence that the type 2 copper centers are the site of nitrite reduction by Achromobacter cycloclastes nitrite reductase. Biochem. Biophys. Res. Commun. 187, 1529-1535
40. Fittipaldi, M., Wijma, H. J., Verbeet, M. P., Canters, G. W., Groenen, E. J. and Huber, M. (2005) The substrate-bound type 2 copper site of nitrite reductase: the nitrogen hyperfine coupling of nitrite revealed by pulsed EPR. Biochemistry 44, 15193-15202 (Pubitemid 41681453)
41. Abraham, Z. H., Smith, B. E., Howes, B. D., Lowe, D. J. and Eady, R. R. (1997) pH-dependence for binding a single nitrite ion to each type-2 copper centre in the copper-containing nitrite reductase of Alcaligenes xylosoxidans. Biochem. J. 324, 511-516 (Pubitemid 27267995)
42. Jacobson, F., Pistorius, A., Farkas, D., De Grip, W., Hansson, O., Sjölin, L. and Neutze, R. (2007) pH dependence of copper geometry, reduction potential, and nitrite affinity in nitrite reductase. J. Biol. Chem. 282, 6347-6355 (Pubitemid 47100846)
43. Wijma, H. J., Jeuken, L. J., Verbeet, M. P., Armstrong, F. A. and Canters, G. W. (2006) A random-sequential mechanism for nitrite binding and active site reduction in copper-containing nitrite reductase. J. Biol. Chem. 281, 16340-16346