A Novel Extracellular Multicopper Oxidase from Phanerochaete chrysosporium with Ferroxidase Activity

Applied and Environmental Microbiology

Volumn 69, Issue 10, 2003, Pages 6257-6263

  Larrondo, Luis F ^a   Salas, Loreto ^a   Melo, Francisco ^a   Vicuña, Rafael ^a   Cullen, Daniel ^b  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b FOREST PRODUCTS LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIODEGRADATION; ELECTROPHORESIS; LIGNIN; OXIDATION; ULTRAVIOLET RADIATION;

LIGNIN DEGRADATION;

ENZYME KINETICS;

AROMATIC AMINE; CERULOPLASMIN; COPPER; FUNGAL ENZYME; GLYOXAL OXIDASE; IRON; LACCASE; LIGNIN; LIGNIN PEROXIDASE; MANGANESE PEROXIDASE; MULTICOPPER OXIDASE; OXIDOREDUCTASE; PHENOL DERIVATIVE; RECOMBINANT PROTEIN; THIAZOLE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS NIDULANS; BASIDIOMYCETES; DEGRADATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SUBSTRATE; FUNGAL GENE; GENOME; MCO1 GENE; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PHANEROCHAETE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; STRUCTURE ANALYSIS; ULTRAVIOLET SPECTROSCOPY;

ASPERGILLUS; BASIDIOMYCOTA; CHRYSOSPORIUM; EMERICELLA NIDULANS; EUKARYOTA; FUNGI; PHANEROCHAETE; PHANEROCHAETE CHRYSOSPORIUM;

EID: 0142040829     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.69.10.6257-6263.2003     Document Type: Article

References (51)

1. Askwith, C., D. Eide, A. Van Ho, P. S. Bernard, L. Li, S. Davis-Kaplan, D. M. Sipe, and J. Kaplan. 1994. The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76:403-410.
2. Askwith, C. C., and J. Kaplan. 1998. Site-directed mutagenesis of the yeast multicopper oxidase Fet3p. J. Biol. Chem. 273:22415-22419.
3. Bao, W., Y. Fukushima, K. A. Jensen, M. A. Moen, and K. E. Hammel. 1994. Oxidative degradation of non-phenolic lignin during lipid peroxidation by fungal manganese peroxidase. FEBS Lett. 354:297-300.
4. Berman, H. M., J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, and P. E. Bourne. 2000. The Protein Data Bank. Nucleic Acids Res. 28:235-242.
5. Bertrand, T., C. Jolivalt, P. Briozzo, E. Caminade, N. Joly, C. Madzak, and C. Mougin. 2002. Crystal structure of a four-copper laccase complexed with an arylamine: insights into substrate recognition and correlation with kinetics. Biochemistry 41:7325-7333.
6. Blanchette, R. 1991. Delignification by wood-decay fungi. Annu. Rev. Phytopathol. 29:381-398.
7. Bonaccorsi di Patti, M. C., M. R. Felice, A. P. Camuti, A. Lania, and G. Musci. 2000. The essential role of Glu-185 and Tyr-354 residues in the ferroxidase activity of Saccharomyces cerevisiae Fet3. FEBS Lett. 472:283-286.
8. Bonaccorsi di Patti, M. C., M. P. Paronetto, V. Dolci, M. R. Felice, A. Lania, and G. Musci. 2001. Mutational analysis of the iron binding site of Saccharomyces cerevisiae ferroxidase Fet3. An in vivo study. FEBS Lett. 508:475-478.
9. Bonomi, F., D. M. Kurtz, and X. Cui. 1996. Ferroxidase activity of recombinant Desulfovibrio vulgaris rubrerythrin. J. Biol. Inorg. Chem. 1:67-72.
10. Bourbonnais, R., and M. G. Paice. 1990. Oxidation of non-phenolic substrates. An expanded role for laccase in lignin biodegradation. FEBS Lett. 267:99-102.
11. de Silva, D., S. Davis-Kaplan, J. Fergestad, and J. Kaplan. 1997. Purification and characterization of Fet3 protein, a yeast homologue of ceruloplasmin. J. Biol. Chem. 272:14208-14213.
12. De Silva, D. M., C. C. Askwith, D. Eide, and J. Kaplan. 1995. The FET3 gene product required for high affinity iron transport in yeast is a cell surface ferroxidase. J. Biol. Chem. 270:1098-1101.
13. Dittmer, J., N. Patel, S. Dhawale, and S. Dhawale. 1997. Production of multiple laccase forms by Phanerochaete chrysosporium grown under nutrient sufficiency. FEMS Microbiol. Lett. 149:65-70.
14. Ducros, V., A. M. Brzozowski, K. S. Wilson, S. H. Brown, P. Ostergaard, P. Schneider, D. S. Yaver, A. H. Pedersen, and G. J. Davies. 1998. Crystal structure of the type-2 Cu-depleted laccase from Coprinus cinereus at 2.2 A resolution. Nat. Struct. Biol. 5:310-316.
15. Eggert, C., U. Temp, and K. Eriksson. 1997. Laccase is essential for lignin degradation by the white-rot fungus Pycnoporus cinnabarinus. FEBS Lett. 407:89-92.
16. Eriksson, K.-E. L., R. A. Blanchette, and P. Ander. 1990. Microbial and enzymatic degradation of wood and wood components. Springer-Verlag, Berlin, Germany.
17. Francis, C. A., E. M. Co, and B. M. Tebo. 2001. Enzymatic manganese(II) oxidation by a marine alpha-proteobacterium. Appl. Environ. Microbiol. 67:4024-4029.
18. Francis, C. A., and B. M. Tebo. 2002. Enzymatic manganese(II) oxidation by metabolically dormant spores of diverse Bacillus species. Appl. Environ. Microbiol. 68:874-880.
19. Gilliland, G., S. Perrin, and H. Bunn. 1990. Competitive PCR for quantitation of mRNA, p. 60-69. In M. Innis, D. Gelfand, J. Sninsky, and T. White (ed.), PCR protocols. Academic Press, New York, N.Y.
20. Hakulinen, N., L. L. Kiiskinen, K. Kruus, M. Saloheimo, A. Paananen, A. Koivula, and J. Rouvinen. 2002. Crystal structure of a laccase from Melano-carpus albomyces with an intact trinuclear copper site. Nat. Struct. Biol. 9:601-605.
21. Hammel, K. E., B. Kalyanaraman, and T. K. Kirk. 1986. Substrate free radicals are intermediates in ligninase catalysis. Proc. Natl. Acad. Sci. USA 83:3808-3812.
22. Harvey, P. J., H. E. Schoemaker, R. M. Bowen, and J. M. Palmer. 1985. Single-electron transfer processes and the reaction mechanism of enzymic degradation of lignin. FEBS Lett. 183:13-16.
23. Hatakka, A. 1994. Lignin-modifying enzymes from selected white-rot fungi: production and role in lignin degradation. FEMS Microbiol. Rev. 13:125-135.
24. Horton, R., H. Hunt, S. Ho, J. Pullen, and L. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
25. Kapich, A. N., K. A. Jensen, and K. E. Hammel. 1999. Peroxyl radicals are potential agents of lignin biodegradation. FEBS Lett. 461:115-119.
26. Kersten, P. J., M. Tien, B. Kalyanaraman, and T. K. Kirk. 1985. The ligninase of Phanerochaete chrysosporium generates cation radicals from methoxybenzenes. J. Biol. Chem. 260:2609-2612.
27. Kersten, P. J., C. Witek, A. Vanden Wymelenberg, and D. Cullen. 1995. Phanerochaete chrysosporium glyoxal oxidase is encoded by two allelic variants: structure, genomic organization and heterologous expression of glx1 and glx2. J. Bacteriol. 177:6106-6110.
28. Kirk, T. K., and R. L. Farrell. 1987. Enzymatic "combustion": the microbial degradation of lignin. Annu. Rev. Microbiol. 41:465-505.
29. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
30. Larrondo, L. F., M. Avila, L. Salas, D. Cullen, and R. Vicuna. 2003. Heterologous expression of laccase cDNA from Ceriporiopsis subvermispora yields copper activated apoprotein and complex isoform patterns. Microbiology 149:1177-1182.
31. Larrondo, L. F., S. Lobos, P. Stewart, D. Cullen, and R. Vicuna. 2001. Isoenzyme multiplicity and characterization of recombinant manganese peroxidases from Ceriporiopsis subvermispora and Phanerochaete chrysosporium. Appl. Environ. Microbiol. 67:2070-2075.
32. Liu, L., R. P. Tewari, and P. R. Williamson. 1999. Laccase protects Cryptococcus neoformans from antifungal activity of alveolar macrophages. Infect. Immun. 67:6034-6039.
33. Lobos, S., J. Larrain, L. Salas, D. Cullen, and R. Vicuna. 1994. Isozymes of manganese-dependent peroxidase and laccase produced by the lignin-degrading basidiomycete Ceriporiopsis subvermispora. Microbiology 140:2691-2698.
34. Marquez, L., H. Wariishi, H. B. Dunford, and M. H. Gold. 1988. Spectroscopic and kinetic properties of oxidized intermediates of lignin peroxidase from Phanerochaete chrysosporium. J. Biol. Chem. 263:10549-10552.
35. Messerschmidt, A., R, Ladenstein, R. Huber, M. Bolognesi, L. Avigliano, R. Petruzzelli, A. Rossi, and A. Finazzi-Agro. 1992. Refined crystal structure of ascorbate oxidase at 1.9 A resolution. J. Mol. Biol. 224:179-205.
36. Piontek, K., M. Antorini, and T. Choinowski. 2002. Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-A resolution containing a full complement of coppers. J. Biol. Chem. 277:37663-37669.
37. Podgornik, H., M. Stegu, E. Zibert, and A. Perdih. 2001. Laccase production by Phanerochaete chrysosporium - an artifact caused by Mn(III)? Lett. Appl. Microbiol. 32:407-411.
38. Rajakumar, S., J. Gaskell, D. Cullen, S. Lobos, E. Karahanian, and R. Vicuna. 1996. Lip-like genes in Phanerochaete sordida and Ceriporiopsis subvermispora, white rot fungi with no detectable lignin peroxidase activity. Appl. Environ. Microbiol. 62:2660-2663.
39. Rodriguez, C. S., R. Santro, C. Cameselle, and A. Sanroman. 1997. Laccase production in semi-solid cultures of Phanerochaete chrysosporium. Biotechnol. Lett. 19:995-998.
40. Sali, A., and T. L. Blundell. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
41. Schoemaker, H. E., P. J. Harvey, R. M. Bowen, and J. M. Palmer. 1985. On the mechanism of enzymatic lignin breakdown. FEBS Lett. 183:7-12.
42. Srinivasan, C., T. D'Souza, K. Boominathan, and C. Reddy. 1995. Demonstration of laccase in the white rot basidiomycete Phanerochaete chrysosporium BKM-F-1767. Appl. Environ. Microbiol. 61:4274-4277.
43. Stearman, R., D. S. Yuan, Y. Yamaguchi-Iwai, R. D. Klausner, and A. Dancis. 1996. A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271:1552-1557.
44. Thurston, C. F. 1994. The structure and function of fungal laccases. Microbiology 140:19-26.
45. Vallim, M. A., B. J. Janse, J. Gaskell, A. A. Pizzirani-Kleiner, and D. Cullen. 1998. Phanerochaete chrysosporium cellobiohydrolase and cellobiose dehydrogenase transcripts in wood. Appl. Environ. Microbiol. 64:1924-1928.
46. Wariishi, H., L. Akileswaran, and M. H. Gold. 1988. Manganese peroxidase from the basidiomycete Phanerochaete chrysosporium: spectral characterization of the oxidized states and the catalytic cycle. Biochemistry 27:5365-5370.
47. Wariishi, H., and M. H. Gold. 1990. Lignin peroxidase compound III. Mechanism of formation and decomposition. J. Biol. Chem. 265:2070-2077.
48. Wartmann, T., U. W. Stephan, I. Bube, E. Boer, M. Melzer, R. Manteuffel, R. Stoltenburg, L. Guengerich, G. Gellissen, and G. Kunze. 2002. Posttranslational modifications of the AFET3 gene product: a component of the iron transport system in budding cells and mycelia of the yeast Arxula adeninivorans. Yeast 19:849-862.
49. Williams, D. M., G. R. Lee, and G. E. Cartwright. 1974. Ferroxidase activity of rat ceruloplasmin. Am. J. Physiol. 227:1094-1097.
50. Williamson, P. R. 1994. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J. Bacteriol. 176:656-664.
51. Wymelenberg, A. V., S. Denman, D. Dietrich, J, Bassett, X. Yu, R. Atalla, P. Predki, U. Rudsander, T. T. Teeri, and D, Cullen. 2002. Transcript analysis of genes encoding a family 61 endoglucanase and a putative membrane-anchored family 9 glycosyl hydrolase from Phanerochaete chrysosporium. Appl. Environ. Microbiol. 68:5765-5768.