Laccase isoforms with unusual properties from the basidiomycete Steccherinum ochraceum strain 1833

Journal of Applied Microbiology

Volumn 105, Issue 6, 2008, Pages 2065-2075

  Chernykh, A ^a   Myasoedova, N ^a   Kolomytseva, M ^a   Ferraroni, M ^b   Briganti, F ^b   Scozzafava, A ^b   Golovleva, L ^a  

^a SKRYABIN INSTITUTE OF BIOCHEMISTRY AND PHYSIOLOGY OF MICROORGANISMS   (Russian Federation)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Laccase; pH stability; Steccherinum ochraceum; Thermostability; White rot fungi

Indexed keywords

ENZYMES; FUNGI; PH EFFECTS; PURIFICATION;

HIGHEST TEMPERATURE; ISOFORMS; LACCASE ISOFORMS; LACCASES; N-TERMINAL AMINO ACID SEQUENCE; PH STABILITY; PH-STABILITY; STECCHERINUM OCHRACEA; SUBSTRATE SPECIFICITY; WHITE ROT FUNGI;

AMINO ACIDS;

ISOENZYME; LACCASE; LACCASE I; LACCASE II; LACCASE III; UNCLASSIFIED DRUG;

ABSORPTION; AMINO ACID; BIOTECHNOLOGY; ENZYME ACTIVITY; EXTINCTION COEFFICIENT; FUNGUS; HIGH TEMPERATURE; PH; PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BASIDIOMYCETES; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME STABILITY; FUNGAL STRAIN; LENTINUS EDODES; MOLECULAR WEIGHT; NONHUMAN; PH; SEQUENCE HOMOLOGY; STECCHERINUM OCHRACEUM; TEMPERATURE DEPENDENCE; THERMOSTABILITY;

FUNGI; LENTINULA EDODES; STECCHERINUM OCHRACEUM;

EID: 56649121998     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2008.03924.x     Document Type: Article

References (69)

1. Alves, A.M., Record, E., Lomascolo, A., Scholtmeijer, K., Asther, M., Wessels, J.G. Wosten, H.A. (2004) Highly efficient production of laccase by the basidiomycete Pycnoporus cinnabarinus. Appl Environ Microbiol 70, 6379 6384.
2. Asiegbu, F.O., Abu, S., Stenlid, J. Johansson, M. (2004) Sequence polymorphism and molecular characterization of laccase genes of the conifer pathogen Heterobasidion annosum. Mycol Res 108, 136 148.
3. Baldrian, P. (2004) Purification and characterization of laccase from the white-rot fungus Daedalea quercina and decolorization of synthetic dyes by the enzyme. Appl Microbiol Biotechnol 63, 560 563.
4. Baldrian, P. (2006) Fungal laccases - occurrence and properties. FEMS Microbiol Rev 30, 215 242.
5. Baldrian, P. Gabriel, J. (2002) Variability of laccase activity in the white-rot basidiomycete Pleurotus ostreatus. Folia Microbiol (Praha) 47, 385 390.
6. Baldrian, P., Valaskova, V., Merhautova, V. Gabriel, J. (2005) Degradation of lignocellulose by Pleurotus ostreatus in the presence of copper, manganese, lead and zinc. Res Microbiol 156, 670 676.
7. Bertrand, T., Jolivalt, C., Briozzo, P., Caminade, E., Joly, N., Madzak, C. Mougin, C. (2002) Crystal structure of a four-copper laccase complexed with an arylamine: insights into substrate recognition and correlation with kinetics. Biochemistry 41, 7325 7333.
8. Bollag, J.M., Shuttleworth, K.L. Anderson, D.H. (1988) Laccase-mediated detoxification of phenolic compounds. Appl Environ Microbiol 54, 3086 3091.
9. Calvo, A., Copapatino, M.J., Alonso, L.O. Gonzalez, A.E. (1998) Studies of the production and characterization of laccase activity in the basidiomycete Coriolopsis gallica, an efficient decolorizer of alkaline effluents. Arch Microbiol 171, 31 36.
10. Casella, L., Gullotti, M., Monzani, E., Santagostini, L., Zoppellaro, G. Sakurai, T. (2006) Enzymatic and spectroscopic studies on the activation or inhibition effects by substituted phenolic compounds in the oxidation of aryldiamines and catechols catalyzed by Rhus vernicifera laccase. J Inorg Biochem 100, 2127 2139.
11. Chefetz, B., Chen, Y. Hadar, Y. (1998) Purification and characterization of laccase from Chaetomium thermophilium and its role in humification. Appl Environ Microbiol 64, 3175 3179.
12. Chernykh, A., Leontievsky, A. Golovleva, L. (2005) New approaches to increasing the yield of laccase from Panus tigrinus. Appl Biochem Microbiol 41, 508 511.
13. Coll, P.M., Fernandez-Abalos, J.M., Villanueva, L.R., Santamaria, R. Perez, P. (1993) Purification and characterization of a phenoloxidase (laccase) from the lignin-degrading basidiomycete PM1(CECT 2971). Appl Environ Microbiol 59, 2607 2613.
14. Couto, S.R. Herrera, J.L.T. (2006) Industrial and biotechnological applications of laccases: a review. Biotechnol Adv 24, 500 513.
15. Dedeyan, B., Klonowska, A., Tagger, S., Tron, T., Iacazio, G., Gil, G. Le Petit, J. (2000) Biochemical and molecular characterization of a laccase from Marasmius quercophilus. Appl Environ Microbiol 66, 925 929.
16. Dong, J.L. Zhang, Y.Z. (2004) Purification and characterization of two laccase isoenzymes from a ligninolytic fungus Trametes gallica. Prep Biochem Biotechnol 34, 179 194.
17. Eggert, C., Temp, U. Eriksson, K.E. (1996) The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus: purification and characterization of the laccase. Appl Environ Microbiol 62, 1151 1158.
18. Farnet, A.M., Criquet, S., Tagger, S., Gil, G. Le Petit, J. (2000) Purification, partial characterization, and reactivity with aromatic compounds of two laccases from Marasmius quercophilus strain 17. Can J Microbiol 46, 189 194.
19. Farnet, A.M., Criquet, S., Pocachard, E., Gil, G. Ferre, E. (2002) Purification of a new isoform of laccase from a Marasmius quercophilus strain isolated from a cork oak litter (Quercus suber L.). Mycologia 94, 735 740.
20. Farnet, A.M., Criquet, S., Cigna, M., Gil, G. Ferre, E. (2004) Purification of a laccase from Marasmius quercophilus induced with ferulic acid: reactivity towards natural and xenobiotic aromatic compounds. Enzyme Microb Technol 34, 549 554.
21. Ferraroni, M., Myasoedova, N.M., Schmatchenko, V., Leontievsky, A.A., Golovleva, L.A., Scozzafava, A. Briganti, F. (2007) Crystal structure of a blue laccase from Lentinus tigrinus: evidences for intermediates in the molecular oxygen reductive splitting by multicopper oxidases. BMC Struct Biol 7, 60.
22. Fields, A. (2001) Review: Protein function at thermal extremes: balancing stability and flexibility. Comp Biochem Physiol Part A 129, 417 431.
23. Fukushima, Y. Kirk, T.K. (1995) Laccase component of the Ceriporiopsis subvermispora lignin-degrading system. Appl Environ Microbiol 61, 872 876.
24. Galhaup, C., Wagner, H., Hinterstoisser, B. Haltrich, D. (2002) Increased production of laccase by wood-degrading basidiomycete Trametes pubescens. Enzyme Microb Technol 30, 529 536.
25. Garzillo, A.M., Colao, M.C., Buonocore, V., Olivia, R., Falcigno, L., Saviano, M., Santoro, A.M., Zappala, R., Bonoma, R.P., Bianco, C., Giardina, P., Palmieri, G. Sannia, G. (2001) Structural and kinetic characterization of native laccases from Pleurotus ostreatus, Rigidoporus lignosus and Trametes trogii. J Prot Chem 20, 191 201.
26. Garzillo, A.M., Dipaolo, V.S., Burla, G. Buonocore, V. (1992) Differently-induced extracellular phenol oxidases from Pleurotus ostreatus. Phytochemistry 31, 3685 3690.
27. Gianfreda, L., Xu, F. Bollag, J.-M. (1999) Laccases: a useful group of oxidoreductive enzymes. Bioremed J 3, 1 25.
28. Goldberg, M., Farver, O. Pecht, I. (1980) Interaction of Rhus laccase with dioxygen and its reduction intermediates. J Biol Chem 255, 7353 7361.
29. Hakala, T.K., Lundell, T., Galkin, S., Maijala, P., Kalkkinen, N. Hatakka, A. (2005) Manganese peroxidases, laccases and oxalic acid from the selective white-rot fungus Physisporinus rivulosus grown on spruce wood chips. Enzyme Microb Technol 36, 461 468.
30. Hakulinen, N., Kruus, K., Koivula, A. Rouvinen, J. (2006) A crystallographic and spectroscopic study on the effect of X-ray radiation on the crystal structure of Melanocarpus albomyces laccase. Biochem Biophys Res Comm 350, 929 934.
31. Hanna, P.M., McMillin, D.R., Pasenkiewich-Gierula, M., Antholine, W.E. Reinhammar, B. (1988a) Type 2-depleted fungal laccase. Biochem J 253, 561 568.
32. Hanna, P.M., Tamilarasan, R. McMillin, D.R. (1988b) Cu(I) analysis of blue copper proteins. Biochem J 256, 1001 1004.
33. Hilden, K., Hakala, T.K., Maijala, P., Lundell, T.K. Hatakka, A. (2007) Novel thermotolerant laccases produced by the white-rot fungus Physisporinus rivulosus. Appl Microbiol Biotechnol 77, 301 309.
34. Iimura, Y., Hartikainen, P. Tatsumi, K. (1996) Dechlorination of tetrachloroguaiacol by laccase of white-rot basidiomicete Coriolus versicolor. Appl Microbiol Biotechnol 45, 434 439.
35. Jung, H., Xu, F. Li, K. (2002) Purification and characterization of laccase from wood-degrading fungus Trichophyton rubrum LKY-7. Enzyme Microbial Technol 30, 161 168.
36. Kaal, E.E., Field, J.A. Joyce, T.W. (1995) Increasing ligninolitic enzyme activities in several white-rot baidiomycetes by nitrogen sufficient media. Bioresour Technol 53, 133 139.
37. Kiiskinen, L.L., Viikari, L. Kruus, K. (2002) Purification and characterization of a novel laccase from the ascomycete Melanocarpus albomyces. Appl Microbiol Biotechnol 59, 198 204.
38. Koroleva, O.V., Stepanova, E.V., Gavrilova, V.P., Yakovleva, N.S., Landesman, E.O., Yavmetdinov, I.S. Yaropolov, A.I. (2002) Laccase and Mn-peroxidase production by Coriolus hirsutus strain 075 in a jar fermenter. J Biosci Bioeng 93, 1 7.
39. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680 685.
40. Larrondo, L.F., Salas, L., Melo, F., Vicuna, R. Cullen, D. (2003) A novel extracellular multicopper oxidase from Phanerochaete chrysosporium with ferroxidase activity. Appl Environ Microbiol 69, 6257 6263.
41. Leonowicz, A. Grzywnowicz, K. (1981) Quantitative estimation of laccase forms in some white-rot fungi using syringaldazine as a substrate. Enzyme Microb Technol 3, 55 58.
42. Leontievsky, A.A., Vares, T., Lankinen, P., Shergill, J.K., Pozdnyakova, N.N., Myasoedova, N.M., Kalkkinen, N., Golovleva, L.A. et al. (1997) Blue and yellow laccases of ligninolytic fungi. FEMS Microbiol Lett 156, 9 14.
43. Leontievsky, A.A., Myasoedova, N.M., Baskunov, B.P., Golovleva, L.A., Bucke, C. Evans, C.S. (2001) Transformation of 2,4,6-trichlorophenol by free and immobilized fungal laccase. Appl Microbiol Biotechnol 57, 85 91.
44. Lineweaver, H. Burk, D. (1934) The determination of enzyme dissociation constants. J Am Chem Soc 56, 658 666.
45. Liu, W., Chao, Y., Liu, S., Bao, H. Qian, S. (2003) Molecular cloning and characterization of a laccase gene from the basidiomycete Fome lignosus and expression in Pichia pastoris. Appl Microbiol Biotechnol 63, 174 181.
46. Lowry, O.H., Rosebrough, N.J., Farr, A.L. Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265 275.
47. Malkin, R., Malmström, B.G. Vänngård, T. (1969) The reversible removal of one specific copper(II) from fungal laccase. Eur J Biochem 7, 253 259.
48. Mikuni, J. Morohoshi, N. (1997) Cloning and sequencing of a second laccase gene from the white-rot fungus Coriolus versicolor. FEMS Microbiol Lett 155, 79 84.
49. Myasoedova, N.M., Chernykh, A.M., Psurtseva, N.V., Belova, N.V. Golovleva, L.A. (2008) New efficient producers of fungal laccases. Appl Biochem Microbiol (Russia) 44, 84 89.
50. Nagai, M., Sato, T., Watanabe, H., Saito, K., Kawata, M. Enei, H. (2002) Purification and characterization of an extracellular laccase from the edible mushroom Lentinula edodes, and decolorization of chemically different dyes. Appl Microbiol Biotechnol 60, 327 335.
51. Palmieri, G., Giardina, P., Bianco, C., Fontanella, B. Sannia, G. (2000) Copper induction of laccase isoenzymes in the ligninolitic fungus Pleurotus ostreatus. Appl Environ Microbiol 66, 920 924.
52. Paszczyński, A., Huynh, V.-B. Crawford, R. (1986) Comparison of ligninase-I and peroxidase-M2 from the white-rot fungus Phanerochuete chrysosporium. Arch Biochem Biophys 244, 750 765.
53. Perez, J. Jeffries, T.W. (1990) Mineralization of C-ring-labeled synthetic lignin correlates with the production of lignin peroxidase, not of manganese peroxidase or laccase. Appl Environ Microbiol 56, 1806 1812.
54. Quaratino, D., Federici, F., Petruccioli, M., Fenice, M. D'Annibale, A. (2007) Production, purification and partial characterisation of a novel laccase from the white-rot fungus Panus tigrinus CBS 577.79. Antonie Van Leeuwenhoek 91, 57 69.
55. Quintanar, L., Stoj, C., Taylor, A.B., Hart, P.J., Kosman, D.J. Solomon, E.I. (2007) Shall we dance? How a multicopper oxidase chooses its electron transfer partner. Acc Chem Rev 40, 445 452.
56. Ruttimann-Johnson, C., Salas, L., Vicuna, R. Kirk, K. (1993) Extracellular enzyme production and synthetic lignin mineralization by Ceriporiopsis subvermispora. Appl Environ Microbiol 59, 1792 1797.
57. Saloheimo, M., Niku-Paavola, M.L. Knowles, J.K. (1991) Isolation and structural analysis of the laccase gene from the lignin-degrading fungus Phlebia radiata. J Gen Microbiol 137, 1537 1544.
58. Saparrat, M.C.N., Bucsinszky, A.M.M., Tounier, H.A., Cabello, M.N. Arambarri, A.M. (2000) Extracellular ABTS-oxidizing activity of a autochthonous gungal strains from Argentina in solid medium. Rev Iberoam Micol 17, 64 68.
59. Schneider, P., Caspersen, M.B., Mondorf, K., Halkier, T., Skov, L.K., Ostergaard, P.R., Brown, K.M., Brown, S.H. et al. (1999) Characterization of a Coprinus cinereus laccase. Enzyme Microb Technol 25, 502 508.
60. Soden, D.M. Dobson, A.D. (2001) Differential regulation of laccase gene expression in Pleurotus sajor-caju. Microbiology 147, 1755 1763.
61. Solomon, E.I., Baldwin, M.J. Lowery, M.D. (1992) Electronic structures of active sites in copper proteins: contributions to reactivity. Chem Rev 92, 521 542.
62. Solomon, E.I., Sundaram, U.M. Machonkin, T.E. (1996) Multicopper oxydases and oxygenases. Chem Rev 96, 2563 2605.
63. Somero, G.N. (2004) Adaptation of enzymes to temperatures: searching for basic 'strategies'. Comp Biochem Physiol B 139, 312 333.
64. Ullah, M.A., Bedford, C.T. Evans, C.S. (2000) Reactions of pentachlorophenol with laccase from Coriolus versicolor. Appl Microbiol Biotechnol 53, 230 234.
65. Wang, H.X. Ng, T.B. (2004a) A novel laccase with fair thermostability from the edible wild mushroom (Albatrella dispansus). Biochem Biophys Res Commun 319, 381 385.
66. Wang, H.X. Ng, T.B. (2004b) Purification of a novel low molecular-mass laccase with HIV-1 reverse transcriptase inhibitory activity from the mushroom Tricholoma giganteum. Biochem Biophys Res Commun 315, 450 454.
67. Xu, F. (1996) Oxidation of phenols, anilines, and benzenethiols by fungal laccases: correlation between activity and redox potentials as well as halide inhibition. Biochemistry 35, 7608 7614.
68. Xu, F., Kulys, J.J., Duke, K., Li, K., Krikstopaitis, K., Deussen, H.-J.W., Abbate, E., Galinyte, V. et al. (2000) Redox chemistry in laccase-catalyzed oxidation of N-hydroxy compounds. Appl Environ Microbiol 66, 2052 2056.
69. Yaver, D.S. Golightly, E.J. (1996) Cloning and characterization of three laccase genes from the white-rot basidiomycete Trametes villosa: genomic organization of the laccase gene family. Gene 181, 95 102.