Identification and Characterization of a Multifunctional Dye Peroxidase from a Lignin-Reactive Bacterium

ACS Chemical Biology

Volumn 7, Issue 12, 2012, Pages 2074-2081

  Brown, Margaret E ^a   Barros, Tiago ^a   Chang, Michelle C Y ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYE; LIGNIN; PEROXIDASE;

AMYCOLATOPSIS; ARTICLE; CRYSTALLOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SOIL MICROFLORA;

BIOMASS; COLORING AGENTS; GRAM-POSITIVE BACTERIA; LIGNIN; MODELS, MOLECULAR; OXIDATION-REDUCTION; PEROXIDASES;

AMYCOLATOPSIS SP.; BACTERIA (MICROORGANISMS);

EID: 84871590888     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300383y     Document Type: Article

References (56)

1. Claassen, P. A. M., van Lier, J. B., Lopez Contreras, A. M., van Niel, E. W. J., Sijtsma, L., Stams, A. J. M., de Vries, S. S., and Weusthuis, R. A. (1999) Utilization of biomass for the supply of energy carriers Appl. Microbiol. Biotechnol. 52, 741-755
2. Greene, N. (2004) Growing energy: How biofuels can help end America's oil dependence, Natural Resources Defense Council, New York.
3. Himmel, M. E., Ding, S.-Y., Johnson, D. K., Adney, W. S., Nimlos, M. R., Brady, J. W., and Foust, T. D. (2007) Biomass recalcitrance: Engineering plants and enzymes for biofuels production Science 315, 804-807
4. Langeveld, J. W. A., Dixon, J., and Jaworski, J. F. (2010) Development perspectives of the biobased economy: A review Crop Sci. 50, S142-S151
5. Ralph, J., Lundquist, K., Brunow, G., Lu, F., Kim, H., Schatz, P. F., Marita, J. M., Hatfield, R. D., Ralph, S. A., Christensen, J. H., and Boerjan, W. (2004) Lignins: Natural polymers from oxidative coupling of 4-hydroxylphenylpropanoids Phytochem. Rev. 3, 29-60
6. Kirk, T. K. and Farrell, R. L. (1987) Enzymatic "combustion": The microbial degradation of lignin Annu. Rev. Microbiol. 41, 465-505
7. ten Have, R. and Teunissen, P. J. (2001) Oxidative mechanisms involved in lignin degradation by white-rot fungi Chem. Rev. 101, 3397-3413
8. Ramachandra, M., Crawford, D. L., and Hertel, G. (1988) Characterization of an extracellular lignin peroxidase of the lignocellulolytic actinomycete Streptomyces viridosporus Appl. Environ. Microbiol. 54, 3057-3063
9. Kirby, R. (2005) Actinomycetes and lignin degradation, in Advances in Applied Microbiology (Laskin, A. I., Bennett, J. W., Gadd, G. M., and Sariaslani, S., Eds.) pp 125-168, Academic Press, London, U.K.
10. Ahmad, M., Taylor, C. R., Pink, D., Burton, K., Eastwood, D., Bending, G. D., and Bugg, T. D. H. (2010) Development of novel assays for lignin degradation: Comparative analysis of bacterial and fungal lignin degraders Mol. BioSyst. 6, 815-821
11. Crawford, D. L., Pometto, A. L., III, and Crawford, R. L. (1983) Lignin degradation by Streptomyces viridosporus: Isolation and characterization of a new polymeric lignin degradation intermediate Appl. Environ. Microbiol. 45, 898-904
12. Brown, M. E., Walker, M. C., Nakashige, T. G., Iavarone, A. T., and Chang, M. C. Y. (2011) Discovery and characterization of heme enzymes from unsequenced bacteria: Application to microbial lignin degradation J. Am. Chem. Soc. 133, 18006-18009
13. Davis, J. R., Goodwin, L. A., Woyke, T., Teshima, Hazuki, Bruce, D., Detter, C., Tapia, R., Han, S., Han, J., Pitluck, S., Nolan, M., Mikhailova, N., Land, M. L., and Sello, J. K. (2012) Genome sequence of A. sp. strain ATCC 39116, a plant biomass-degrading actinomycete J. Bacteriol. 194, 2396-2397
14. Sugano, Y. (2009) DyP-type peroxidases comprise a novel heme peroxidase family Cell. Mol. Life Sci. 66, 1387-1403
15. Johjima, T., Ohkuma, M., and Kudo, T. (2003) Isolation and cDNA cloning of novel hydrogen peroxide-dependent phenol oxidase from the basidiomycete Termitomyces albuminosus Appl. Microbiol. Biotechnol. 61, 220-225
16. Sugano, Y., Muramatsu, R., Ichiyanagi, A., Sato, T., and Shoda, M. (2007) DyP, a unique dye-decolorizing peroxidase, represents a novel heme peroxidase family J. Biol. Chem. 282, 36652-36658
17. Scheibner, M., Hülsdau, B., Zelena, K., Nimtz, M., de Boer, L., Berger, R., and Zorn, H. (2008) Novel peroxidases of Marasmius scorodonius degrade β-carotene Appl. Microbiol. Biotechnol. 77, 1241-1250
18. 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
19. 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
20. Li, J., Liu, C., Li, B., Yuan, H., Yang, J., and Zheng, B. (2012) Identification and molecular characterization of a novel DyP-type peroxidase from Pseudomonas aeruginosa PKE117 Appl. Biochem. Biotechnol. 166, 774-785
21. Roberts, J. N., Singh, R., Grigg, J. C., Murphy, M. E. P., Bugg, T. D. H., and Eltis, L. D. (2011) Characterization of dye-decolorizing peroxidases from Rhodococcus jostii RHA1 Biochemistry 50, 5108-5119
22. Ahmad, M., Roberts, J. N., Hardiman, E. M., Singh, R., Eltis, L. D., and Bugg, T. D. H. (2011) Identification of DypB from Rhodococcus jostii RHA1 as a lignin peroxidase Biochemistry 50, 5096-5107
23. 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
24. 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: Struct., Funct., Bioinf. 69, 223-233
25. Sato, T., Hara, S., Matsui, T., Sazaki, G., Saijo, S., Ganbe, T., Tanaka, N., Sugano, Y., and Shoda, M. (2004) A unique dye-decolorizing peroxidase, DyP, from Thanatephorus cucumeris Dec 1: Heterologous expression, crystallization and preliminary X-ray analysis Acta Crystallogr., Sect. D 60, 149-152
26. Battistuzzi, G., Bellei, M., Bortolotti, C. A., and Sola, M. (2010) Redox properties of heme peroxidases Arch. Biochem. Biophys. 500, 21-36
27. Sugano, Y., Matsushima, Y., and Shoda, M. (2006) Complete decolorization of the anthraquinone dye Reactive Blue 5 by the concerted action of two peroxidases from Thanatephorus cucumeris Dec 1 Appl. Microbiol. Biotechnol. 73, 862-871
28. Heinfling, A., Ruiz-Dueñas, F. J., Martínez, M. J., Bergbauer, M., Szewzyk, U., and Martínez, A. T. (1998) A study on reducing substrates of manganese-oxidizing peroxidases from Pleurotus eryngii and Bjerkandera adusta FEBS Lett. 428, 141-146
29. 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., 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: Struct., Funct., Bioinf. 69, 234-243
30. Fernández-Fueyo, E., Ruiz-Dueñas, F. J., Miki, Y., Martínez, M. J., Hammel, K. E., and Martínez, A. T. (2012) Lignin-degrading peroxidases from genome of selective ligninolytic fungus Ceriporiopsis subvermispora J. Biol. Chem. 287, 16903-16916
31. Kuan, I. C., Johnson, K. A., and Tien, M. (1993) Kinetic analysis of manganese peroxidase. The reaction with manganese complexes J. Biol. Chem. 268, 20064-20070
32. Banci, L., Camarero, S., Martínez, A., Martínez, M., Pérez-Boada, M., Pierattelli, R., and Ruiz-Dueñas, F. (2003) NMR study of manganese(II) binding by a new versatile peroxidase from the white-rot fungus Pleurotus eryngii J. Biol. Inorg. Chem. 8, 751-760
33. Katayama, T., Nakatsubo, F., and Higuchi, T. (1981) Syntheses of arylglycerol-β-aryl ethers Mokuzai Gakkaishi 27, 223-230
34. Wei, K., Luo, S.-W., Fu, Y., Liu, L., and Guo, Q.-X. (2004) A theoretical study on bond dissociation energies and oxidation potentials of monolignols J. Mol. Struct.: THEOCHEM 712, 197-205
35. Tien, M. and Ma, D. (1997) Oxidation of 4-methoxymandelic acid by lignin peroxidase J. Biol. Chem. 272, 8912-8917
36. Baciocchi, E., Gerini, M. F., Lanzalunga, O., and Mancinelli, S. (2002) Lignin peroxidase catalysed oxidation of 4-methoxymandelic acid. The role of mediator structure Tetrahedron 58, 8087-8093
37. Yamazaki, I. and Piette, L. H. (1963) The mechanism of aerobic oxidase reaction catalyzed by peroxidase Biochim. Biophys. Acta 77, 47-64
38. Paszczynski, A., Huynh, V.-B., and Crawford, R. (1986) Comparison of ligninase-I and peroxidase-M2 from the white-rot fungus Phanerochaete chrysosporium Arch. Biochem. Biophys. 244, 750-765
39. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797
40. Singh, R., Grigg, J. C., Armstrong, Z., Murphy, M. E. P., and Eltis, L. D. (2012) Distal heme pocket residues of B-type dye-decolorizing peroxidase: Arginine but not aspartate is essential for peroxidase activity J. Biol. Chem. 287, 10623-10630
41. Sundaramoorthy, M., Youngs, H., Gold, M. H., and Poulos, T. L. (2005) High-resolution crystal structure of manganese peroxidase: Substrate and inhibitor complexes Biochemistry 44, 6463-6470
42. Pérez-Boada, M., Ruiz-Dueñas, F. J., Pogni, R., Basosi, R., Choinowski, T., Martínez, M. J., Piontek, K., and Martínez, A. T. (2005) Versatile peroxidase oxidation of high redox potential aromatic compounds: Site-directed mutagenesis, spectroscopic and crystallographic investigation of three long-range electron transfer pathways J. Mol. Biol. 354, 385-402
43. The UniProt Consortium (2012) Reorganizing the protein space at the Universal Protein Resource (UniProt) Nucleic Acids Res. 40, D71-D75
44. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res. 25, 3389-3402
45. Armougom, F., Moretti, S., Poirot, O., Audic, S., Dumas, P., Schaeli, B., Keduas, V., and Notredame, C. (2006) Expresso: Automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee Nucleic Acids Res. 34, W604-W608
46. Notredame, C., Higgins, D. G., and Heringa, J. (2000) T-coffee: A novel method for fast and accurate multiple sequence alignment J. Mol. Biol. 302, 205-217
47. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 28, 2731-2739
48. Makino, R., Park, S.-y., Obayashi, E., Iizuka, T., Hori, H., and Shiro, Y. (2011) Oxygen binding and redox properties of the heme in soluble guanylate cyclase J. Biol. Chem. 286, 15678-15687
49. Dutton, P. L. (1978) Redox potentiometry: Determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems Methods Enzymol. 54, 411-435
50. Kabsch, W. (2010) XDS Acta Crystallogr., Sect. D 66, 125-132
51. Collaborative Computational Project No. 4 (1994) The CCP4 suite: Programs for protein crystallography, Acta Crystallogr., Sect. D 50, 760-763.
52. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
53. Zhang, K. Y. J., Cowtan, K., and Main, P. (1997) Combining constraints for electron-density modification Methods Enzymol. 277, 53-64
54. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G. W., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments Acta Crystallogr., Sect. D 67, 235-242
55. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr., Sect. D 60, 2126-2132
56. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D 66, 213-221