Characterization of dye-decolorizing peroxidases from rhodococcus jostii RHA1

Biochemistry

Volumn 50, Issue 23, 2011, Pages 5108-5119

  Roberts, Joseph N ^a   Singh, Rahul ^a   Grigg, Jason C ^a   Murphy, Michael E P ^a   Bugg, Timothy D H ^b   Eltis, Lindsay D ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC RESIDUES; ANTHRAQUINONE DYE; AXIAL POSITIONS; COMPOUND I; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; EPR SPECTRA; HEME IRON; HEME PROPIONATES; LIGNIN DEGRADATION; PEROXIDASE ACTIVITIES; REACTIVE BLUE 4; RESTING STATE; RHODOCOCCUS; SECOND-ORDER RATE CONSTANTS; SOIL BACTERIUM; SOLVENT SPECIES; STEADY-STATE KINETICS; X RAY CRYSTAL STRUCTURES;

ABSORPTION SPECTROSCOPY; AMINO ACIDS; CRYSTAL STRUCTURE; DEGRADATION; KETONES; LIGNIN; MANGANESE; MANGANESE COMPOUNDS; PARAMAGNETIC RESONANCE; PARAMAGNETISM; PLANTS (BOTANY); PORPHYRINS; RATE CONSTANTS; SOLVENTS;

ELECTRON SPIN RESONANCE SPECTROSCOPY;

2,2' AZINOBIS(3 ETHYLBENZOTHIAZOLINE 6 SULFONIC ACID); LIGNIN; PEROXIDASE; PROTEIN DYPA; PROTEIN DYPB; PYROGALLOL; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RHODOCOCCUS; RHODOCOCCUS JOSTII; STEADY STATE;

ANTHRAQUINONES; COLORING AGENTS; ELECTRON SPIN RESONANCE SPECTROSCOPY; KINETICS; OXIDATION-REDUCTION; PEROXIDASES; RHODOCOCCUS; SPECTROPHOTOMETRY, ULTRAVIOLET;

BACTERIA (MICROORGANISMS); RHODOCOCCUS JOSTII;

EID: 79958818206     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200427h     Document Type: Article

References (63)

1. Kim, S. J. and Shoda, M. (1999) Purification and characterization of a novel peroxidase from Geotrichum candidum Dec 1 involved in decolorization of dyes Appl. Environ. Microbiol. 65, 1029-1035 (Pubitemid 29111167)
2. Sugano, Y. (2009) DyP-type peroxidases comprise a novel heme peroxidase family Cell. Mol. Life Sci. 66, 1387-1403
3. Sugano, Y., Muramatsu, R., Ichiyanagi, A., Sato, T., and Shoda, M. (2007) DyP, a unique dye-decolorizing peroxidase, represents a novel heme peroxidase family: ASP171 replaces the distal histidine of classical peroxidases J. Biol. Chem. 282, 36652-36658
4. Ogola, H. J. O., Kamiike, T., Hashimoto, N., Ashida, H., Ishikawa, T., Shibata, H., and Sawa, Y. (2009) Molecular Characterization of a Novel Peroxidase from the Cyanobacterium Anabaena sp. Strain PCC 7120 Appl. Environ. Microbiol. 75, 7509-7518
5. Liers, C., Bobeth, C., Pecyna, M., Ullrich, R., and Hofrichter, M. (2010) DyP-like peroxidases of the jelly fungus Auricularia auricula-judae oxidize nonphenolic lignin model compounds and high-redox potential dyes Appl. Microbiol. Biotechnol. 85, 1869-1879
6. Sugano, Y., Sasaki, K., and Shoda, M. (1999) cDNA cloning and genetic analysis of a novel decolorizing enzyme, peroxidase gene dyp from Geotrichum candidum Dec 1 J. Biosci. Bioeng. 87, 411-417 (Pubitemid 29239000)
7. Sugano, Y., Matsushima, Y., Tsuchiya, K., Aoki, H., Hirai, M., and Shoda, M. (2009) Degradation pathway of an anthraquinone dye catalyzed by a unique peroxidase DyP from Thanatephorus cucumeris Dec 1 Biodegradation 20, 433-440
8. van Bloois, E., Pazmino, D. E. T., Winter, R. T., and Fraaije, M. W. (2010) A robust and extracellular heme-containing peroxidase from Thermobifida fusca as prototype of a bacterial peroxidase superfamily Appl. Microbiol. Biotechnol. 86, 1419-1430
9. Zelena, K., Zorn, H., Nimtz, M., and Berger, R. G. (2009) Heterologous expression of the msp2 gene from Marasmius scorodonius Arch. Microbiol. 191, 397-402
10. Kaur, A., Van, P. T., Busch, C. R., Robinson, C. K., Pan, M., Pang, W. L., Reiss, D. J., Diruggiero, J., and Baliga, N. S. (2010) Coordination of frontline defense mechanisms under severe oxidative stress Mol. Syst. Biol. 6, 393
11. Kong, L., Guo, D., Zhou, S., Yu, X., Hou, G., Li, R., and Zhao, B. (2010) Cloning and expression of a toxin gene from Pseudomonas fluorescens GcM5-1A Arch. Microbiol. 192, 585-593
12. Letoffe, S., Heuck, G., Delepelaire, P., Lange, N., and Wandersman, C. (2009) Bacteria capture iron from heme by keeping tetrapyrrol skeleton intact Proc. Natl. Acad. Sci. U.S.A. 106, 11719-11724
13. Sutter, M., Boehringer, D., Gutmann, S., Gunther, S., Prangishvili, D., Loessner, M. J., Stetter, K. O., Weber-Ban, E., and Ban, N. (2008) Structural basis of enzyme encapsulation into a bacterial nanocompartment Nat. Struct. Mol. Biol. 15, 939-947
14. Ogola, H. J., Hashimoto, N., Miyabe, S., Ashida, H., Ishikawa, T., Shibata, H., and Sawa, Y. (2010) Enhancement of hydrogen peroxide stability of a novel Anabaena sp. DyP-type peroxidase by site-directed mutagenesis of methionine residues Appl. Microbiol. Biotechnol. 87, 1727-1736
15. Sturm, A., Schierhorn, A., Lindenstrauss, U., Lilie, H., and Bruser, T. (2006) YcdB from Escherichia coli reveals a novel class of TAT-dependently translocated hemoproteins J. Biol. Chem. 281, 13972-13978 (Pubitemid 43848323)
16. Zubieta, C., Joseph, R., Krishna, S. S., McMullan, D., Kapoor, M., Axelrod, H. L., Miller, M. D., Abdubek, P., Acosta, C., Astakhova, T., Carlton, D., Chiu, H. J., Clayton, T., Deller, M. C., Duan, L., Elias, Y., Elsliger, M. A., Feuerhelm, J., Grzechnik, S. K., Hale, J., Han, G. W., Jaroszewski, L., Jin, K. K., Klock, H. E., Knuth, M. W., Kozbial, P., Kumar, A., Marciano, D., Morse, A. T., Murphy, K. D., Nigoghossian, E., Okach, L., Oommachen, S., Reyes, R., Rife, C. L., Schimmel, P., Trout, C. V., van den Bedem, H., Weekes, D., White, A., Xu, Q. P., Hodgson, K. O., Wooley, J., Deacon, A. M., Godzik, A., Lesley, S. A., and Wilson, I. A. (2007) Identification and structural characterization of heme binding in a novel dye-decolorizing peroxidase, TyrA Proteins 69, 234-243 (Pubitemid 47429287)
17. Poulos, T. L. and Kraut, J. (1980) The stereochemistry of peroxidase catalysis J. Biol. Chem. 255, 8199-8205
18. Yam, K. C., Okamoto, S., Roberts, J. N., and Eltis, L. D. (2011) Adventures in Rhodococcus: From steroids to explosives Can. J. Microbiol. 57, 155-168
19. van der Geize, R. and Dijkhuizen, L. (2004) Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications Curr. Opin. Microbiol. 7, 255-261 (Pubitemid 38758066)
20. Seto, M., Masai, E., Ida, M., Hatta, T., Kimbara, K., Fukuda, M., and Yano, K. (1995) Multiple polychlorinated biphenyl transformation systems in the Gram-positive bacterium Rhodococcus sp. strain RHA1 Appl. Environ. Microbiol. 61, 4510-4513
21. McLeod, M. P., Warren, R. L., Hsiao, W. W., Araki, N., Myhre, M., Fernandes, C., Miyazawa, D., Wong, W., Lillquist, A. L., Wang, D., Dosanjh, M., Hara, H., Petrescu, A., Morin, R. D., Yang, G., Stott, J. M., Schein, J. E., Shin, H., Smailus, D., Siddiqui, A. S., Marra, M. A., Jones, S. J., Holt, R., Brinkman, F. S., Miyauchi, K., Fukuda, M., Davies, J. E., Mohn, W. W., and Eltis, L. D. (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse Proc. Natl. Acad. Sci. U.S.A. 103, 15582-15587 (Pubitemid 44625635)
22. Ahmad, M., Taylor, C. R., Pink, D., Burton, K., Eastwood, D., Bending, G. D., and Bugg, T. D. (2010) Development of novel assays for lignin degradation: Comparative analysis of bacterial and fungal lignin degraders Mol. BioSyst. 6, 815-821
23. Falk, J. E. (1964) Porphyrins and metalloporphyrins; their general, physical and coordination chemistry, and laboratory methods, Elsevier Publishing Co., Amsterdam.
24. Childs, R. E. and Bardsley, W. G. (1975) Steady-State Kinetics of Peroxidase with 2,2-Azino-Di-(3-Ethylbenzthiazoline-6-Sulphonic Acid) as Chromogen Biochem. J. 145, 93-103
25. Hiner, A. N. P., Rodriguez-Lopez, J. N., Arnao, M. B., Raven, E. L., Garcia-Canovas, F., and Acosta, M. (2000) Kinetic study of the inactivation of ascorbate peroxidase by hydrogen peroxide Biochem. J. 348, 321-328 (Pubitemid 30345204)
26. Vickers, T. J. and Fairlamb, A. H. (2004) Trypanothione S-transferase activity in a trypanosomatid ribosomal elongation factor 1B J. Biol. Chem. 279, 27246-27256 (Pubitemid 38812563)
27. Wariishi, H., Valli, K., and Gold, M. H. (1992) Manganese(II) Oxidation by Manganese Peroxidase from the Basidiomycete Phanerochaete-Chrysosporium: Kinetic Mechanism and Role of Chelators J. Biol. Chem. 267, 23688-23695 (Pubitemid 23088173)
28. Cornish-Bowden, A. (1995) Analysis of enzyme kinetic data, Oxford University Press, Oxford, U.K.
29. Van Duyne, G. D., Standaert, R. F., Karplus, P. A., Schreiber, S. L., and Clardy, J. (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin J. Mol. Biol. 229, 105-124 (Pubitemid 23037917)
30. Kabsch, W. (2010) XDS Acta Crystallogr. D66, 125-132
31. Evans, P. (2006) Scaling and assessment of data quality Acta Crystallogr. D62, 72-82
32. Terwilliger, T. C. and Berendzen, J. (1999) Automated MAD and MIR structure solution Acta Crystallogr. D55, 849-861 (Pubitemid 29194533)
33. Terwilliger, T. C. (2000) Maximum-likelihood density modification Acta Crystallogr. D56, 965-972 (Pubitemid 30622779)
34. Terwilliger, T. C. (2003) Automated main-chain model building by template matching and iterative fragment extension Acta Crystallogr. D59, 38-44 (Pubitemid 36117204)
35. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132 (Pubitemid 41742764)
36. Painter, J. and Merritt, E. A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion Acta Crystallogr. D62, 439-450
37. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255 (Pubitemid 27235885)
38. Collaborative Computational Project Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
39. Leslie, A. G. W. (1992) Joint CCP4 and ESFEACMB Newsletter on Protein Crystallography, Vol. 26.
40. Vagin, A. and Teplyakov, A. (2010) Molecular replacement with MOLREP Acta Crystallogr. D66, 22-25
41. Peisach, J., Blumberg, W. E., Ogawa, S., Rachmilewitz, E. A., and Oltzik, R. (1971) The effects of protein conformation on the heme symmetry in high spin ferric heme proteins as studied by electron paramagnetic resonance J. Biol. Chem. 246, 3342-3355
42. Webb, S. M., Dick, G. J., Bargar, J. R., and Tebo, B. M. (2005) Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II) Proc. Natl. Acad. Sci. U.S.A. 102, 5558-5563 (Pubitemid 40530296)
43. Dunford, H. B. (1999) Heme peroxidases, John Wiley, New York.
44. de Geus, D. C., Thomassen, E. A., Hagedoorn, P. L., Pannu, N. S., van Duijn, E., and Abrahams, J. P. (2009) Crystal structure of chlorite dismutase, a detoxifying enzyme producing molecular oxygen J. Mol. Biol. 387, 192-206
45. Zhang, Y. and Skolnick, J. (2005) TM-align: A protein structure alignment algorithm based on the TM-score Nucleic Acids Res. 33, 2302-2309 (Pubitemid 41439897)
46. Babor, M., Gerzon, S., Raveh, B., Sobolev, V., and Edelman, M. (2008) Prediction of transition metal-binding sites from apo protein structures Proteins 70, 208-217 (Pubitemid 350293461)
47. Zubieta, C., Krishna, S. S., Kapoor, M., Kozbial, P., McMullan, D., Axelrod, H. L., Miller, M. D., Abdubek, P., Ambing, E., Astakhova, T., Carlton, D., Chiu, H. J., Clayton, T., Deller, M. C., Duan, L., Elsliger, M. A., Feuerhelm, J., Grzechnik, S. K., Hale, J., Hampton, E., Han, G. W., Jaroszewski, L., Jin, K. K., Klock, H. E., Knuth, M. W., Kumar, A., Marciano, D., Morse, A. T., Nigoghossian, E., Okach, L., Oommachen, S., Reyes, R., Rife, C. L., Schimmel, P., van den Bedem, H., Weekes, D., White, A., Xu, Q., Hodgson, K. O., Wooley, J., Deacon, A. M., Godzik, A., Lesley, S. A., and Wilson, I. A. (2007) Crystal structures of two novel dye-decolorizing peroxidases reveal a β-barrel fold with a conserved heme-binding motif Proteins 69, 223-233 (Pubitemid 47429286)
48. Chance, M., Powers, L., Poulos, T., and Chance, B. (1986) Cytochrome c peroxidase compound ES is identical with horseradish peroxide compound I in iron-ligand distances Biochemistry 25, 1266-1270
49. Khindaria, A. and Aust, S. D. (1996) EPR detection and characterization of lignin peroxidase porphyrin -cation radical Biochemistry 35, 13107-13111 (Pubitemid 26349461)
50. Patterson, W. R., Poulos, T. L., and Goodin, D. B. (1995) Identification of a porphyrin -cation radical in ascorbate peroxidase compound I Biochemistry 34, 4342-4345
51. Liu, X., Du, Q., Wang, Z., Zhu, D., Huang, Y., Li, N., Wei, T., Xu, S., and Gu, L. (2011) Crystal structure and biochemical features of EfeB/YcdB from Escherichia coli O157: Asp235 plays divergent roles in different enzyme-catalyzed processes J. Biol. Chem. 286, 14922-14931
52. Sundaramoorthy, M., Kishi, K., Gold, M. H., and Poulos, T. L. (1994) The crystal structure of manganese peroxidase from Phanerochaete chrysosporium at 2.06-Å resolution J. Biol. Chem. 269, 32759-32767
53. Kishi, K., Kusters-van Someren, M., Mayfield, M. B., Sun, J., Loehr, T. M., and Gold, M. H. (1996) Characterization of manganese(II) binding site mutants of manganese peroxidase Biochemistry 35, 8986-8994 (Pubitemid 26243741)
54. Petruccioli, M., Frasconi, M., Quaratino, D., Covino, S., Favero, G., Mazzei, F., Federici, F., and D'Annibale, A. (2009) Kinetic and redox properties of MnP II, a major manganese peroxidase isoenzyme from Panus tigrinus CBS 577.79 J. Biol. Inorg. Chem. 14, 1153-1163
55. Mester, T. and Field, J. A. (1998) Characterization of a novel manganese peroxidase-lignin peroxidase hybrid isozyme produced by Bjerkandera species strain BOS55 in the absence of manganese J. Biol. Chem. 273, 15412-15417 (Pubitemid 28298146)
56. Ivancich, A., Jakopitsch, C., Auer, M., Un, S., and Obinger, C. (2003) Protein-based radicals in the catalase-peroxidase of Synechocystis PCC6803: A multifrequency EPR investigation of wild-type and variants on the environment of the heme active site J. Am. Chem. Soc. 125, 14093-14102 (Pubitemid 37420914)
57. Carpena, X., Wiseman, B., Deemagarn, T., Singh, R., Switala, J., Ivancich, A., Fita, I., and Loewen, P. C. (2005) A molecular switch and electronic circuit modulate catalase activity in catalase-peroxidases EMBO Rep. 6, 1156-1162 (Pubitemid 41741699)
58. Ortiz de Montellano, P. R. (1992) Catalytic sites of hemoprotein peroxidases Annu. Rev. Pharmacol. Toxicol. 32, 89-107
59. Sivaraja, M., Goodin, D. B., Smith, M., and Hoffman, B. M. (1989) Identification by ENDOR of Trp191 as the free-radical site in cytochrome c peroxidase compound ES Science 245, 738-740 (Pubitemid 19214005)
60. Singh, R., Switala, J., Loewen, P. C., and Ivancich, A. (2007) Two [Fe(IV) - O Trp*] intermediates in M. tuberculosis catalase-peroxidase discriminated by multifrequency (9-285 GHz) EPR spectroscopy: Reactivity toward isoniazid J. Am. Chem. Soc. 129, 15954-15963
61. Sundaramoorthy, M., Terner, J., and Poulos, T. L. (1995) The crystal structure of chloroperoxidase: A heme peroxidase-cytochrome P450 functional hybrid Structure 3, 1367-1377 (Pubitemid 3012264)
62. Nagano, S., Tanaka, M., Ishimori, K., Watanabe, Y., and Morishima, I. (1996) Catalytic roles of the distal site asparagine-histidine couple in peroxidases Biochemistry 35, 14251-14258 (Pubitemid 26384420)
63. Jakopitsch, C., Auer, M., Regelsberger, G., Jantschko, W., Furtmuller, P. G., Ruker, F., and Obinger, C. (2003) The catalytic role of the distal site asparagine-histidine couple in catalase-peroxidases Eur. J. Biochem. 270, 1006-1013 (Pubitemid 36315344)