Abstract
Recently, the structure of a Cu-containing nitrite reductase (NiR) from Hyphomicrobium denitrificans (HdNiR) has been reported, establishing the existence of a new family of Cu-NiR where an additional type 1 Cu (T1Cu) containing cupredoxin domain is located at the N-terminus (Nojiri et al. in Proc. Natl. Acad. Sci. USA 104:4315–4320, 2007). HdNiR retains the well-characterised coupled T1Cu–type 2 Cu (T2Cu) core, where the T2Cu catalytic site is also built utilising ligands from neighbouring monomers. We have undertaken a genome analysis and found the wide occurrence of these NiRs, with members clustering in two groups, one showing an amino acid sequence similarity of around 80% with HdNiR, and a second group, including the NiR from the extremophile Acidothermus cellulolyticus, clustering around 50% similarity to HdNiR. This is reminiscent of the difference observed between the blue (Alcaligenes xylosoxidans) and green (Achromobacter cycloclastes and Alcaligenes faecalis) NiRs which have been extensively studied and may indicate that these also form two distinct subclasses of the new family. Genome analysis also showed the presence of Cu-NiRs with a C-terminal extension of 160–190 residues containing a class I cytochrome c domain with a characteristic β-sheet extension. Currently no structural information exists for any member of this family. Genome analysis suggests the widespread occurrence of these novel NiRs with representatives in the α, β and γ subclasses of the Proteobacteria and in two species of the fungus Aspergillus. We selected the enzyme from Ralstonia pickettii for comparative modelling and produced a plausible structure highlighting an electron transfer mode in which the cytochrome c haem at the C-terminus can come within 16-Å reach of the T1Cu centre of the T1Cu–T2Cu core.
Similar content being viewed by others
Notes
The nomenclature for abbreviating different NiRs follows the binomial convention in which the first letter (in capital) signifies the genus and second letter denotes the species, e.g. Achromobacter cycloclastes NiR becomes AcNiR. If the abbreviation is ambiguous then the second letter of the species is added, e.g. AceNiR for Acidothermus cellulolyticus NiR.
Ralstonia pickettii is a nonfermenting gram-negative bacillus of relatively low virulence that is often associated with pseudobacteremia or asymptomatic colonisation of patients. Contamination of water supplies, skin disinfectants, and saline solutions used either for patient care or for laboratory diagnosis has previously been incriminated. Ralstonia pickettii is resistant to some antiseptics and is able to survive in an oligotrophic environment [10, 11].
Abbreviations
- AceNiR:
-
Acidothermus cellulolyticus nitrite reductase
- AcNiR:
-
Achromobacter cycloclastes nitrite reductase
- AfNiR:
-
Alcaligenes faecalis S6 nitrite reductase
- AxNiR:
-
Alcaligenes xylosoxidans nitrite reductase
- BbNiR:
-
Bdellovibrio bacteriovorus nitrite reductase
- BCP:
-
Blue copper protein
- CgNiR:
-
Chaetomium globosum nitrite reductase
- CvNiR:
-
Chromobacterium violaceum nitrite reductase
- HdNiR:
-
Hyphomicrobium denitrificans nitrite reductase
- NgNiR:
-
Neisseria gonorrhoeae nitrite reductase
- NiR:
-
Nitrite reductase
- PHYRE:
-
Protein Homology/analogY Recognition Engine
- RpNiR:
-
Ralstonia pickettii 12J nitrite reductase
- T1Cu:
-
Type 1 copper
- T2Cu:
-
Type 2 copper
References
Nojiri M, Xie Y, Inoue T, Yamamoto T, Matsumura H, Kataoka K, Deligeer, Yamaguchi K, Kai Y, Suzuki S (2007) Proc Natl Acad Sci USA 104:4315–4320
Eady RR, Hasnain SS (2003) In: McCleverty JA, Meyer TJ (eds) Comprehensive coordination chemistry II. Elsevier, Oxford, pp 759–786
Antonyuk S, Strange RW, Sawers G, Eady RR, Hasnain SS (2005) Proc Natl Acad Sci USA 102:12041–12046
Boulanger MJ, Murphy MEP (2002) J Mol Biol 315:1111–1127
Ellis MJ, Dodd FE, Sawers G, Eady RR, Hasnain SS (2003) J Mol Biol 328:429–438
Murphy MEP, Turley S, Kukimoto M, Nishiyama M, Horinouchi S, Sasaki H, Tanokura M, Adman ET (1995) Biochemistry 34:12107–12117
Pinho D, Besson S, Brondino CD, De Castro B, Moura I (2004) Eur J Biochem 271:2361–2369
Zumft WG, Gotzmann DJ, Kroneck PM (1987) Eur J Biochem 168:301–307
Bertini I, Cavallaro G, Rosato A (2006) Chem Rev 106:90–115
Barbut F, Kosmann MJ, Lalande V, Neyme D, Coppo P, Gorin NC (2006) Infect Control Hosp Epidemiol 27:642–644
Ryan MP, Pembroke JT, Adley CC (2006) J Hosp Infect 62:278–284
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Nucleic Acids Res 25:3389–3402
Pearson WR (1990) Methods Enzymol 183:63–98
Pearson WR, Lipman DJ (1988) Proc Natl Acad Sci USA 85:2444–2448
Thompson JD, Higgins DG, Gibson TJ (1994) Nucleic Acids Res 22:4673–4680
Rice P, Longden I, Bleasby A (2000) Trends Genet 16:276–277
Kelley LA, Maccallum RM, Sternberg MJ (2000) J Mol Biol 299:499–520
Jacobson F, Guo H, Olesen K, Okvist M, Neutze R, Sjolin L (2005) Acta Crystallogr D Biol Crystallogr 61:1190–1198
Than ME, Hof P, Huber R, Bourenkov GP, Bartunik HD, Buse G, Soulimane T (1997) J Mol Biol 271:629–644
Williams P, Coates L, Mohammed F, Gill R, Erskine P, Bourgeois D, Wood SP, Anthony C, Cooper JB (2006) J Mol Biol 357:151–162
Muresanu L, Pristovsek P, Lohr F, Maneg O, Mukrasch MD, Ruterjans H, Ludwig B, Lucke C (2006) J Biol Chem 281:14503–14513
Chen L, Durley RC, Mathews FS, Davidson VL (1994) Science 264:86–90
Chen R, Li L, Weng Z (2003) Proteins 52:80–87
Sippl MJ (1993) Proteins 17:355–362
Wiederstein M, Sippl MJ (2007) Nucleic Acids Res 35:W407–W410
Karlin KD, Zhu ZY, Karlin S (1998) J Biol Inorg Chem 3:172–187
Karlin S, Zhu ZY, Karlin KD (1997) Proc Natl Acad Sci USA 94:14225–14230
Godoy D, Randle G, Simpson AJ, Aanensen DM, Pitt TL, Kinoshita R, Spratt BG (2003) J Clin Microbiol 41:2068–2079
Chen ZW, Matsushita K, Yamashita T, Fujii TA, Toyama H, Adachi O, Bellamy HD, Mathews FS (2002) Structure 10:837–849
Oubrie A, Rozeboom HJ, Kalk KH, Huizinga EG, Dijkstra BW (2002) J Biol Chem 277:3727–3732
Simon J, Einsle O, Kroneck PM, Zumft WG (2004) FEBS Lett 569:7–12
Gon S, Giudici-Orticoni MT, Mejean V, Iobbi-Nivol C (2001) J Biol Chem 276:11545–11551
Kanbi LD, Antonyuk SV, Hough MA, Hall JF, Dodd FE, Hasnain SS (2002) J Mol Biol 320:263–275
Nakamura K, Go N (2005) Cell Mol Life Sci 62:2050–2066
Nakamura K, Kawabata T, Yura K, Go N (2003) FEBS Lett 553:239–244
Delano WL (2002) http://www.pymol.org
Acknowledgements
We would like to thank Michael Hough for his assistance with the theoretical docking program.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ellis, M.J., Grossmann, J.G., Eady, R.R. et al. Genomic analysis reveals widespread occurrence of new classes of copper nitrite reductases. J Biol Inorg Chem 12, 1119–1127 (2007). https://doi.org/10.1007/s00775-007-0282-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00775-007-0282-2