Unexpected diversity of chlorite dismutases: A catalytically efficient dimeric enzyme from Nitrobacter winogradskyi

Journal of Bacteriology

Volumn 193, Issue 10, 2011, Pages 2408-2417

  Mlynek, Georg ^a,b   Sjöblom, Björn ^a   Kostan, Julius ^a   Füreder, Stephanie ^a   Maixner, Frank ^a,d   Gysel, Kira ^a,b   Furtmüller, Paul Georg ^b   Obinger, Christian ^b   Wagner, Michael ^a   Daims, Holger ^a   Djinović Carugo, Kristina ^a,c  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

^d INSTITUTE FOR RENEWABLE ENERGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORITE DISMUTASE; ENZYME; HETERODIMER; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CHEMOLITHOAUTOTROPH; CRYSTAL STRUCTURE; CRYSTALLIZATION; GEL PERMEATION CHROMATOGRAPHY; NITRITE OXIDIZER; NITROBACTER; NITROBACTER WINOGRADSKYI; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL;

CHLORIDES; CRYSTALLOGRAPHY, X-RAY; GENETIC VARIATION; KINETICS; MODELS, MOLECULAR; NITROBACTER; OXIDOREDUCTASES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS); NITROBACTER WINOGRADSKYI; NITROSPIRA;

EID: 79956072032     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01262-10     Document Type: Article

References (47)

1. Adams, P. D., et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66:213-221.
2. Balk, M., T. van Gelder, S. A. Weelink, and A. J. M. Stams. 2008. (Per)chlorate reduction by the thermophilic bacterium, Moorella perchloratireducens sp. nov., isolated from an underground gas storage. Appl. Environ. Microbiol. 74:403-409.
3. Bender, K. S., M. R. Rice, W. H. Fugate, J. D. Coates, and L. A. Achenbach. 2004. Metabolic primers for detection of (per)chlorate-reducing bacteria in the environment and phylogenetic analysis of cld gene sequences. Appl. Environ. Microbiol. 70:5651-5658.
4. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
5. Bendtsen, J. D., H. Nielsen, D. Widdick, T. Palmer, and S. Brunak. 2005. Prediction of twin-arginine signal peptides. BMC Bioinform. 6:167.
6. Cladera, A. M., E. Garcia-Valdes, and J. Lalucat. 2006. Genotype versus phenotype in the circumscription of bacterial species: the case of Pseudomonas stutzeri and Pseudomonas chloritidismutans. Arch. Microbiol. 184:353-361.
7. Coates, J. D., and L. A. Achenbach. 2004. Microbial perchlorate reduction: rocket-fueled metabolism. Nat. Rev. Microbiol. 2:569-580.
8. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
9. Collette, T. W., et al. 2003. Analysis of hydroponic fertilizer matrixes for perchlorate: comparison of analytical techniques. Analyst 128:88-97.
10. Davis, I. W., L. W. Murray, J. S. Richardson, and D. C. Richardson. 2004. MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32:W615-W619.
11. de Geus, D. C., et al. 2009. Crystal structure of chlorite dismutase, a detoxifying enzyme producing molecular oxygen. J. Mol. Biol. 387:192-206.
12. Ebihara, A., et al. 2005. Structure-based functional identification of a novel heme-binding protein from Thermus thermophilus HB8. J. Struct. Funct. Genomics 6:21-32.
13. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
14. Ettwig, K. F., et al. 2010. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543-548.
15. Gasteiger, E., et al. 2005. Protein identification and analysis tools on the ExPASy server, p. 571-607. In J. M. Walker (ed.), The proteomics protocols handbook. Humana Press, Totowa, NJ.
16. Goblirsch, B. R., B. R. Streit, J. L. Dubois, and C. M. Wilmot. 2010. Structural features promoting dioxygen production by Dechloromonas aromatica chlorite dismutase. J. Biol. Inorg. Chem. 15:879-888.
17. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
18. Hynes, R. K., and R. Knowles. 1983. Inhibition of chemoautotrophic nitrification by sodium chlorate and sodium chlorite: a reexamination. Appl. Environ. Microbiol. 45:1178-1182.
19. John, P. 1977. Aerobic and anaerobic bacterial respiration monitored by electrodes. J. Gen. Microbiol. 98:231-238.
20. Kabsch, W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Cryst. 26:795-800.
21. Kirstein, K., and E. Bock. 1993. Close genetic relationship between Nitrobacter hamburgensis nitrite oxidoreductase and Escherichia coli nitrate reductases. Arch. Microbiol. 160:447-453.
22. Kostan, J., et al. 2010. Structural and functional characterisation of the chlorite dismutase from the nitrite-oxidizing bacterium "Candidatus Nitrospira defluvii": Identification of a catalytically important amino acid residue. J. Struct. Biol. 172:331-342.
23. Krissinel, E., and K. Henrick. 2007. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372:774-797.
24. Krissinel, E., and K. Henrick. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60:2256-2268.
25. Kristjansson, J. K., and T. C. Hollocher. 1979. Substrate binding site for nitrate reductase of Escherichia coli is on the inner aspect of the membrane. J. Bacteriol. 137:1227-1233.
26. Kucera, I. 2006. Interference of chlorate and chlorite with nitrate reduction in resting cells of Paracoccus denitrificans. Microbiology 152:3529-3534.
27. Kucera, I. 2003. Passive penetration of nitrate through the plasma membrane of Paracoccus denitrificans and its potentiation by the lipophilic tetraphenylphosphonium cation. Biochim. Biophys. Acta 1557:119-124.
28. Lee, A. Q., B. R. Streit, M. J. Zdilla, M. M. Abu-Omar, and J. L. DuBois. 2008. Mechanism of and exquisite selectivity for O-O bond formation by the hemedependent chlorite dismutase. Proc. Natl. Acad. Sci. U. S. A. 105:15654-15659.
29. Lees, H., and J. R. Simpson. 1957. The biochemistry of the nitrifying organisms. V. Nitrite oxidation by Nitrobacter. Biochem. J. 65:297-305.
30. Logan, B. E., et al. 2001. Kinetics of perchlorate- and chlorate-respiring bacteria. Appl. Environ. Microbiol. 67:2499-2506.
31. Lücker, S., et al. 2010. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc. Natl. Acad. Sci. U. S. A. 107:13479-13484.
32. Ludwig, W., et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
33. Maixner, F., et al. 2008. Environmental genomics reveals a functional chlorite dismutase in the nitrite-oxidizing bacterium 'Candidatus Nitrospira defluvii.' Environ. Microbiol. 10:3043-3056.
34. Mehboob, F., et al. 2009. Purification and characterization of a chlorite dismutase from Pseudomonas chloritidismutans. FEMS Microbiol. Lett. 293:115-121.
35. Painter, J., and E. A. Merritt. 2006. Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 62:439-450.
36. Sen, D., et al. 2010. Comparative genomics of pAKD4, the prototype IncP-1delta plasmid with a complete backbone. Plasmid 63:98-107.
37. Smith, K. M. 1975. Porphyrins and metalloporphyrins. Elsevier Scientific, Amsterdam, Netherlands.
38. Spieck, E., and E. Bock. 2005. The lithoautotrophic nitrite-oxidizing bacteria, p. 149-153. In J. T. Staley, D. R. Boone, D. J. Brenner, P. de Vos, G. M. Garrity, M. Goodfellow, N. R. Krieg, F. A. Rainey, and K. H. Schleifer (ed.), Bergey's manual of systematic bacteriology, 2nd ed., vol. 2. Springer Science+Business Media, New York, NY.
39. Stanbury, J. B., and J. B. Wyngaarden. 1952. Effect of perchlorate on the human thyroid gland. Metabolism 1:533-539.
40. Starkenburg, S. R., et al. 2006. Genome sequence of the chemolithoautotrophic nitrite-oxidizing bacterium Nitrobacter winogradskyi Nb-255. Appl. Environ. Microbiol. 72:2050-2063.
41. Stenklo, K., H. D. Thorell, H. Bergius, R. Aasa, and T. Nilsson. 2001. Chlorite dismutase from Ideonella dechloratans. J. Biol. Inorg. Chem. 6:601-607.
42. Streit, B. R., and J. L. DuBois. 2008. Chemical and steady-state kinetic analyses of a heterologously expressed heme dependent chlorite dismutase. Biochemistry 47:5271-5280.
43. i{dotless} from Nitrobacter agilis and characterization of nitrite oxidation system of the bacterium. Arch. Microbiol. 135:265-271.
44. Ueno, H., K. Oishi, Y. Sayato, and K. Nakamuro. 2000. Oxidative cell damage in Kat-sod assay of oxyhalides as inorganic disinfection by-products and their occurrence by ozonation. Arch. Environ. Contam. Toxicol. 38:1-6.
45. -. Environ. Sci. Technol. 36:2783-2788.
46. van Ginkel, C. G., G. B. Rikken, A. G. Kroon, and S. W. Kengen. 1996. Purification and characterization of chlorite dismutase: a novel oxygen-generating enzyme. Arch. Microbiol. 166:321-326.
47. van Wijk, D. J., S. G. Kroon, and I. C. Garttener-Arends. 1998. Toxicity of chlorate and chlorite to selected species of algae, bacteria, and fungi. Ecotoxicol. Environ. Saf. 40:206-211.