The importance of laccase-mediator systems in lignin degradation

Indian Journal of Microbiology

Volumn 40, Issue 3, 2000, Pages 149-161

  Li, Kaichang ^a   Eriksson, Karl Erik L ^b  

^a OREGON STATE UNIVERSITY   (United States)

^b University of Georgia ^*  (United States)

Author keywords

Fungi; Laccase; Laccase mediators; Lignin degradation; Pulp bleaching

Indexed keywords

EID: 0011655374     PISSN: 00468991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (115)

1. Eriksson K-E, Blanchette RA & Ander P (1990) Microbial and enzymatic degradation of wood and wood components. New York: Springer-Verlag.
2. Keyser P, Kirk TK & Zeikus JG (1978) Ligninolytic system of Phanerochaete chrysosporium: synthesized in the absence of lignin response to nitrogen starvation. J. Bacteriol. 135:790-797.
3. Tien M & Kirk TK (1983) Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium Burds. Science 221:661-663.
4. 2-requiring enzyme preparation involved in lignin biodegradation by the white rot basidiomycete Phanerochaete chrysosporium. Biochem. Biophys. Res. Commun. 114:1077-1083.
5. 2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett. 169:247-250.
6. Eggert C, Temp U & Eriksson K-EL (1996) Laccase-producing white-rot fungus lacking lignin peroxidase and manganese peroxidase. American Chemical Society. Washington, D. C.
7. Hatakka A (1994) Lignin-modifying enzymes from selected white-rot fungi: production and role in lignin degradation. FEMS Microbiol. Rev. 13:125-135.
8. Périé FH & Gold MH (1991) Manganese regulation of Manganese peroxidase expression and lignin degradation by the white rot fungus Dichomitus squalens. Appl. Environ. Microbiol. 57:2240-2245.
9. Jensen KA, Jr., Bao W, Kawai S, Srebotnik E & Hammel KE (1996) Manganese-dependent cleavage of nonphenolic lignin structures by Ceriporiopsis subvermispora in the absence of lignin peroxidase. Appl. Environ. Microbiol. 62:3679-3686.
10. Rüttimann-Johnson C, Schwember E, Salas L, Cullen D & Vicuna R (1992) Ligninolytic enzymes of the white rot basidiomycetes Phlebia brevispora and Ceriporiopsis subvermispora. Biotechnol. Appl. Biochem. 16:64-76.
11. de Jone E, de Vries FP, Field JA, Zwan RP & de Bont JAM (1992) Isolation of basidiomycetes with high peroxidase activity. Mycol. Res. 96:1098-1104.
12. Bermek H, Li K & Eriksson K-EL (1998) Laccase-less mutants of the white-rot fungus Pycnoporus cinnabarinus cannot delignify kraft pulp. J. Biotechnol. 66:117-124.
13. Ander P & Eriksson K-E (1977) Selective degradation of wood components by white rot fungi. Plant Physiol. 41:239-248.
14. 14C-labelled poplar wood lignin by selected white-rot fungi. Eur. J. Appl. Microbiol. Biotechnol. 17:235-242.
15. Eggert C, Temp U, Dean JFD & Eriksson K-EL (1996) A fungal metabolite mediates degradation of nonphenolic lignin structures and synthetic lignin by laccase. FEBS Lett. 391:144-148.
16. Eggert C, Temp U & Eriksson K-EL (1997) Laccase is essential for lignin degradation by the white-rot fungus Pycnoporus cinnabarinus. FEBS Lett. 407:89-92.
17. Bourbonnais R & Paice MG (1990) Oxidation of nonphenolic substrates: An expanded role for laccase in lignin biodegradation. FEBS Lett. 267:99-102.
18. Bourbonnais R & Paice MG (1996) Enzymatic deligninfication of kraft pulp using laccase and a mediator. TAPPI J. 79:199-204.
19. Mayer AM (1987) Polyphenol oxidases in plants -recent progress. Phytochem. 26:11-20.
20. Thomas BR, Yonekura M, Morgan TD, Czapla TH, Hopkins TL & Kramer KJ (1989) A trypsin-solubilized laccase from pharate pupal integument of the tobacco hornworm Manduca sexta. Insect Biochem. 19:611-622.
21. Messerschmidt A, ed. (1997) Multi-copper oxidases. In: Multi-copper oxidases, World Scientific: Singapore.
22. Reinhammar B (1984) Laccase, In: Copper proteins and copper enzymes, (Lonties R, Ed). CRC Press: Boca Raton, Florida, pp. 1-35.
23. Yaropolov AI, Skorobogat'ko OV, Vartanov SS & Varfolomeyev SD (1994) Laccase: properties, catalytic mechanism, and application. Appl. Biochem. Biotechnol. 49:257-280.
24. Thurston CF (1994) The structure and function of fungal laccases. Microbiol. 140:19-26.
25. Solomon EI, Sundaram UM & Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem. Rev. 96:2563-2605.
26. Xu F, (1999) Laccase, In: Encyclopedia of bioprocess technology: fermentation, biocatalysis, and bioseparation, (Flickinger MC & Drew SW, Eds)., John Wiley & Sons, Inc. pp. 1545-1554.
27. O' Malley DM, Whetten R, Bao W, Chen C-L & Sederoff RR (1993) The role of laccase in lignification. Plant J. 4:751-757.
28. Sbaghi M, Jeandet P, Bessis R & Leroux P (1996) Degradation of stilbene-type phytoalexins in relation to the pathogenicity of Botrytis cinerea to grapevines. Plant Pathol. 45:139-144.
29. Machuca A & Duran N (1993) Phenol oxidases production and wood degradation by a thermophilic fungus Thermoascus aurantiacus. Biotechnol. Appl. Biochem. 43:37-44.
30. Williamson PR (1994) Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: Identificaion as a laccase. J. Bacteriol. 176:656-664.
31. Williamson PR, Wakamatsu K & Shosuke I (1998) Melanin biosynthesis in Cryptococcus neoformans. J. Bacteriol. 180:1570-1572.
32. 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.
33. Minuth W, Klischies M & Esser K (1978) The phenoloxidases of the ascomycete Podospora anserina. Biochemisty 90:73-82.
34. Slomczynski D, Nakas JP & Tanenbaum SW (1995) Production and characterization of laccase from Botrytis cinerea 61-34. Appl. Environ. Microbiol. 61:907-912.
35. Morpurgo L (1987) The copper sites of laccases. Life Chem Reports 5:277-288.
36. Palmieri G, Giardina P, Bianco C, Scaloni A, Capasso A & Sannia G (1997) A novel white laccase from Pleurotus ostreaus. J. Biol. Chem. 272:31301-31307.
37. Ducros V, Brzozowski AM, Wilson KS, H. BS, Østergaard P, Scheider P, Yaver DS, Pedersen AH & Davies GJ (1998) Crystal structure of the type-2 Cu depleted laccase from Coprinus cinereus at 2.2 Å resolution. Nat. Struct. Biol. 5:310-316.
38. Solomon EI, Machonkin TE & Sundaram UM, (1997) Spectroscopy of multi-copper oxidases, In: Multicopper oxidases, (Messerschmidt A, Ed). World Scientific, Singapore, pp. 103-128.
39. Messerschmidt A (1998) Metal sites in small blue copper proteins, blue copper oxidases and vanadium-containing enzymes. Structure & Bonding 90:37-68.
40. Canters GW & Gilardi G (1993) Engineering type 1 copper site in proteins. FEBS Lett. 325:39-48.
41. Jonsson L, Sjöstrom K, Haggstrom I & Nyman PO (1995) Characterization of a laccase gene from the white-rot fungus Trames versicolor and structural features of basidiomycete laccases. Biochim. Biophys. Acta 1251:210-215.
42. Xu F, Berka RM, Wahleithner JA, Nelson BA, Shuster JR, Brown SH, Palmer AE & Solomon EI (1998) Site-directed mutations in fungal laccase: effect on redox potential, activity, and pH profile. Biochem. J. 334:63-70.
43. Xu F, Palmer AE, Yaver DS, Berka RM, Gambetta GA, Brown SH & Solomon EI (1999) Targeted mutations in a Trametes villosa laccase. Axial perturbations of the T1 copper. J. Biol. Chem. 274:12372-12375.
44. Reinhammar BRM (1972) Oxidation-reduction potentials of the electron acceptors in laccases and stellacyanin. Biochim. Biophys. Acta 275:245-259.
45. Xu F, Shin W, Brown SH, Wahleithner JA, Sundaram UM & Solomon EI (1996) A study of a series of recombinant fungal laccases and bilirubin oxidase that exhibit significant differences in redox potential, substrate specificity, and stability [published erratum appears in Biochim Biophys Acta 1997 Aug 15;1341(1):99]. Biochim Biophys Acta 1292:303-311.
46. Xu F, Shin W, Brown SH, Wahleithner JA, Sundaram UM & Solomon EI (1996) A study of a series of recombinant fungal laccases and bilirubin oxidase that exhibit significant differences in redox potential, substrate specificity, and stability [published erratum appears in Biochim Biophys Acta 1997 Aug 15;1341(1):99]. Biochim Biophys Acta 1292:303-311.
47. Xu F (1996) Catalysis of novel enzymatic iodide oxidation by fungal laccase. Appl. Biochem. Biotechnol. 59:221-230.
48. Malmström BG, (1965) Two forms of copper in copper-containing oxidases, In: Oxidases and related redox systems, (King TE, Mason HS & Morrison M, Eds)., Wiley, New York. pp. 207-216.
49. Malmström BG (1994) Rack-induced bonding in blue-copper proteins. Eur. J. Biochem. 223:711-718.
50. Amann M (1997) The lignozym process - coming closer to the mill. In: 9th International Symposium on Wood and Pulping Chemistry. Montreal, Canada.
51. Adler E (1977) Lignin chemistry - past, present and future. Wood Sci. Technol. 11:169-218.
52. Sakakibara A, (1983) In: Recent advances in lignin biodegradation research, (Higuchi M, Chang H-M & Kirk TK, Eds)., UNI Publisher, Tokyo, pp. 12-33.
53. Leontievsky A, Myasoedova N, Pozdnyakova N & Golovleva L (1997) 'Yellow' laccase of Panus tigrinus oxidizes non-phenolic substrates without electron-transfer mediators. FEBS Lett. 413:446-448.
54. Leontievsky AA, Vares T, Lankinen P, Shergill JK, Pozdnyakova NN, Myasoedova NM, Kalkkinen N, Golovleva LA, Cammack R, Thurston CF & Hatakka A (1997) Blue and yellow laccases of ligninolytic fungi. FEMS Microbiol Lett 156:9-14.
55. Higuchi T, (1985) Degradative pathways of lignin model compounds, In: Biosynthesis and biodegradation of wood components, (Higuchi T, Ed.). Academic Press. pp. 557-576.
56. Morohoshi N & Haraguchi T (1987) Degradation of lignin by the extracellular enzymes of Coriolus versicolor VI: degradation of syringylglycerol-β-syringyl ether by laccase III-c purified from laccase III by isoelectric focusing. Mokuzai Gakkaishi 33:495-502.
57. Wariishi H, Morohoshi N & Haraguchi T (1987) Degradation of lignin by the extracellular enzymes cf Coriolus versicolor VII: effective degradation of syringyl type β-aryl ether lignin model compound by laccase III. Mokuzai Gakkaishi 33:892-898.
58. β cleavage of phenolic β-1 lignin substructure model compound by laccase of Coriolus versicolor. Mokuzai Gakkaishi 33:792-797.
59. Kawai S, Umezawa T & Higuchi T (1988) Degradation mechanisms of phenolic β-1 lignin substructure model compounds by laccase of Coriolus versicolor. Arch. Biochem Biophys 262:99-110.
60. Kawai S, Umezawa T, Shimada M & Higuchi T (1988) Aromatic ring cleavage of 4,6-di(tert-butyl)guaiacol, a phenolic lignin model compound, by laccase of Coriolus versicolor. FEBS Lett. 2:309-311.
61. Bourbonnais R & Paice MG (1992) Demethylation and delignification of kraft pulp by laccase of Trametes versicolor. Appl. Microbiol. Biotechnol. 36:823-827.
62. Pedersen G & Schmidt M (1992) International patent 9218687.
63. Sariaslani FS, Beale JM, Jr. & Rosazza JP (1984) Oxidation of rotenone by Polyporus anceps laccase. J. Nat. Prod. 47:692-697.
64. Kawai S, Umezawa T & Higuchi T (1989) Oxidation of methoxylated benzyl alcohols by laccase of Coriolus versicolor in the presence of syringaldehyde. Wood Research 76:10-16.
65. Bourbonnais R, Paice MG, Reid ID, Lanthier P & Yaguchi M (1995) Lignin oxidation by laccase isozymes from Trametes versicolor and role of the mediator 2,2′-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymerization. Appl. Environ. Microbiol. 61:1876-1880.
66. Call HP & Mucke I (1994) State of the art of enzyme bleaching, disclosure of a breakthough process. In: TAPPI conference. San Diego, USA.
67. Call HP & Mücke I (1997) History, overview and applications of mediated lignolytic systems, especially laccase-mediator-systems (Lignozym®-process). J. Biotechnol. 53:163-202.
68. Archibald FS, Bourbonnais R, Jurasek L, Paice MG & Reid ID (1997) Kraft pulp bleaching and delignification by Trametes versicolor. J. Biotechnol. 53:215-236.
69. Bourbonnais R, Paice MG, Freiermuth B, Bodie E & Borneman S (1997) Reactivities of various mediators and laccases with kraft pulp and lignin model compounds. Appl. Environ. Microbiol. 63:4627-4632.
70. Li K, Prabhu NG, Cooper DA, Xu F, Elder T & Eriksson K-EL, (2000) Development of New Laccase-mediators for Pulp Bleaching, In: Fundamentals and Catalysis of Oxidative Delignification Process, (Argyropoulos DS, Ed.) In press.
71. Bourbonnais R, Rochefort D, Paice MG, Renaud S & Leech D (2000) Development of stable redox complexes to mediate delignification of kraft pulp by laccase. In: 219th ACS national meeting. San Francisco, USA.
72. Bourbonnais R, Rochefort D, Paice MG, Renaud S & Leech D (1999) PCT World patent application, WO 99/54545.
73. Bourbonnais R, Rochefort D, Paice MG, Renaud S & Leech D, (2000) Development of stable redox complexes to mediate delignification of kraft pulp by laccase, In: Fundamentals and catalysis of oxidative delignification process, (Argyropoulos DS, Ed.) In press.
74. Li K, Xu F & Eriksson KE (1999) Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl. Environ. Microbiol. 65:2654-2660.
75. Potthast A, Rosenau T, Chen CL & Gratzl JS (1995) Selective Enzymatic oxidation of aromatic methyl-groups to aldehydes. J. Org. Chem. 60:4320-4321.
76. Potthast A, Rosenau T, Chen CL & Gratzl JS (1996) A novel method for the conversion of benzyl alcohols to benzaldehydes by laccase-catalyzed oxidation. J. Mol. Catal. A-Chem. 108:5-9.
77. Majcherczyk A, Johannes C & Hüttermann A (1999) Oxidation of aromatic alcohols by laccase from Trametes versicolor mediated by the 2,2′-azino-bis-(3-ethylbenzothiazoline-6-sulphonic acid) cation radical and dication. Appl. Microbiol. Biotechnol. 51:267-276.
78. Muheim A, Fiechter A, Harvey PJ & Schoemaker HE (1992) On the mechanism of oxidation of non-phenolic lignin model compounds by the laccase-ABTS couple. Holzforschung 46:121-126.
79. Balakshin MY, Chen CL, Gratzl JS, Kirkman AG & Jakob H (2000) Kinetic studies on oxidation of veratryl alcohol by laccase-mediator system. Part 1. Effects of mediator concentration. Holzforschung 54:165-170.
80. Balakshin MY, Chen CL, Gratzl JS, Kirkman AG & Jakob H (2000) Kinetic studies on oxidation of veratryl alcohol by laccase-mediator system. Part 2. The kinetics of dioxygen uptake. Holzforschung 54:171-175.
81. Li K, Helm RF & Eriksson K-EL (1998) Mechanistic studies of the oxidation of a non-phenolic lignin model compound by the laccase/1-hydroxybenzotriazole redox system. Botechnol. Appl. Biochem. 27:239-243.
82. Hosaya S & Nakano J (1980) Reaction of α-carbonyl group in lignin during alkaline hydrogen peroxide bleaching. Mokuzai Gakkaishi 26:97.
83. Li K, Bermek K & Eriksson K-E (1997) A new technique for screening of laccase-mediators. In: Biological Sciences Symposium. San Francisco, USA.
84. th ACS National Meeting. Anaheim, CA.
85. Kawai S, Asukai M, Ohya N, Okita K, Ito T & Ohashi H (1999) Degradation of a non-phenolic β-O-4 substructure and of polymeric lignin model compounds by laccase of Coriolus versicolor in the presence of 1-hydroxybenzotriazole. FEMS Microbiol. Lett. 170:51-57.
86. Kawai S, Nakagawa M & Ohashi H (1999) Aromatic ring cleavage of a non-phenolic β-O-4 lignin model dimer by laccase of Trametes versicolor in the presence of 1-hydroxybenzotriazole. FEBS Lett. 446:355-358.
87. Sealey J & Ragauskas AJ (1998) Residual lignin studies of laccase-delignified kraft pulps. Enzyme Microb. Technol. 23:422-426.
88. Potthast A, Koch H & Fischer K (1997) The laccase-mediator-system - Reaction with model compounds and pulp. In: 9th International Symposium on Wood and Pulping Chemistry. Montreal, Canada.
89. Sealey J & Ragauskas AJ (1998) Investigation of laccase/N-hydroxybenzotriazole delignification of kraft pulp. J. Wood Chem. Technol. 18:403-416.
90. Jakob H, Grosso MD, Küver A, Nimmerfroh N & Süss HU (1999) Delignification of chemical pulp with laccase and mediators - a concept with a future? Papier 53:85-95.
91. + for calculation of one-electron redox potentials of antioxidants. J. Phys. Chem. 95:10824-10827.
92. Bourbonnais R, Leech D & Paice MG (1998) Electrochemical analysis of the interactions of laccase mediators with lignin model compounds. Biochim. Biophys. Acta. 1379:381-390.
93. Xu F, Kulys JJ, Duke K, Li K, Krikstopaitis K, Deussen HJ, Abbate E, Galinyte V & Schneider P (2000) Redox Chemistry in Laccase-Catalyzed Oxidation of N-Hydroxy Compounds. Appl. Environ. Microbiol. 66:2052-2056.
94. 3+ catalyzed by a fungal laccase. FEBS Lett. 451:186-190.
95. Cui F & Dolphin D (1990) The role of manganese in model systems related to lignin biodegradation. Holzforschung 44:279-283.
96. Kersten PJ, Kalyanaraman B, Hammel KE, Reinhammar B & Kirk TK (1990) Comparison of lignin peroxidase, horseradish peroxidase and laccase in the oxidation of methoxybenzenes. Biochem. J. 268:475-480.
97. Eggert C, Temp U, Dean JF & Eriksson K-EL (1995) Laccase-mediated formation of the phenoxazinone derivative, cinnabarinic acid. FEBS Lett. 376:202-206.
98. Li K, Horanyi P, Collins R, Phillips RS & Eriksson K-EL (2000) Investigation of the role of 3-hydroxyanthranilic acid in the degradation of lignin by white-rot fungus Pycnoporus cinnabarinus. Enzyme Microb. Technol. In press.
99. Johannes C & Majcherczyk A (2000) Natural mediators in the oxidation of polycyclic aromatic hydrocarbons by laccase mediator systems. Appl. Environ. Microbiol. 66:524-528.
100. Kremer SM & Wood PM (1992) Evidence that cellobiose oxidase from Phanerochaete chrysoporium is primarily an Fe(III) oxidase. Eur. J. Biochem. 205:133-138.
101. Guillén F, Martínez MJ, Muñoz C & Martínez AT (1997) Quinone redox cycling in the ligninolytic fungus Pleurotus eryngii leading to extracellular production of superoxide anion radical. Arch. Biochem. Biophys. 339:190-199.
102. Guillén F, Muñoz C, Gómez-Toribio V, Martínez AT & Jesus Martínez M (2000) Oxygen activation during oxidation of methoxyhydroquinones by laccase from Pleurotus eryngii. Appl. Environ. Microbiol. 66:170-175.
103. 2+ oxidation. Appl. Environ. Microbiol. 63:2166-2174.
104. Leonowicz A, Matuszewska A, Luterek J, Ziegenhagen D, Wojtas-Wasilewska M, Cho NS, Hofrichter M & Rogalski J (1999) Biodegradation of lignin by white rot fungi. Fungal Genet. Biol. 27:175-185.
105. Ardon O, Kerem Z & Hadar Y (1996) Enhancement of laccase activity in liquid cultures of the ligninolytic fungus Pleurotus ostreatus by cotton stalk extract. J. Biotechnol. 51:201-207.
106. Sealey J, Ragauskas AJ & Elder TJ (1999) Investigations into laccase-mediator delignification of kraft pulps. Holzforschung 53:498-502.
107. Nelson PJ, Chin CWJ, Viikari L & Tenkanen M (1998) The use of a laccase mediator stage in bleaching eucalypt kraft pulps. Appita J. 51:451-455.
108. Poppius-Levlin K, Wang W, Ranua M, Niku-Paavola M-L & Viikari L (1997) Bleaching of chemical pulps by laccase/mediator systems. In: TAPPI Biological Science Symposium. San Francisco, USA.
109. Poppius-Levlin K, Wang W, Tamminen T, Hortling B, Viikari L & Niku-Paavola M-L (1997) Effects of laccase/HBT treatment on pulp and lignin structures. In: 9th International Symposium on Wood and Pulping Chemistry. Montreal, Canada.
110. Tamminen TT, Kleen AM, Ohra-aho TE & Poppiuslevlin KJ (1999) Chemistry of mediated laccase delignification analysed by pyrolysis-GC/MS. 217th ACS National Meeting. Anaheim, CA.
111. Hunt K, Lee CL, Bourbonnais R & Paice MG (1998) Pulp bleaching with dimethyldioxirane and lignin-oxidizing enzymes. J. Pulp Pap. Sci. 24:55-59.
112. Paice MG, Bourbonnais R & Reid ID (1995) Bleaching kraft pulps with oxidative-enzymes and alkaline hydrogen-peroxide. TAPPI J. 78:161-169.
113. Freudenreich J, Amann M, Fritz-Langhals & Stohrer J (1998) Understanding the Lignozym™-process. In: International pulp bleaching conference. Helsinki, Finland.
114. Oksanen T, Amann M, Candussio A, Buchert J & Viikari L (1997) Role of xylanase in laccase-mediator delignification of kraft pulps. In: 9th International Symposium on Wood and Pulping Chemistry. Montreal, Canada.
115. Viikari L, Oksanen T, Buchert J, Amann M & Candussio A (1999) Combined action of hemicellulases and oxidases in bleaching. In: 10th International symposium on wood and pulping chemistry main symposium. Yokohama, Japan.