Laccases for biorefinery applications: a critical review on challenges and perspectives

Bioprocess and Biosystems Engineering

Volumn 38, Issue 12, 2015, Pages 2285-2313

  Roth, Simon ^a   Spiess, Antje C ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Biomass; Biorefinery; Laccase; Lignin; Mediator

Indexed keywords

BIOCONVERSION; BIOMASS; CELLULOSE; CHEMICAL COMPOUNDS; DEGRADATION; DETOXIFICATION; ENZYMATIC HYDROLYSIS; LIGNIN; REFINING;

BIOREFINERIES; CATALYTIC PERFORMANCE; LACCASES; LIGNOCELLULOSIC BIOMASS; MEDIATOR; OXIDATIVE ELIMINATION; OXIDATIVE MODIFICATION; POLYMERIZATION ACTIVITY;

ENZYMES;

LACCASE; LIGNIN;

BIOMASS; ENZYME SPECIFICITY; METABOLISM; POLYMERIZATION;

BIOMASS; LACCASE; LIGNIN; POLYMERIZATION; SUBSTRATE SPECIFICITY;

EID: 84947864494     PISSN: 16157591     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00449-015-1475-7     Document Type: Review

References (209)

1. Kamm B, Kamm M (2004) Principles of biorefineries. Appl Microbiol Biotechnol 64:137-145
2. Graham-Rowe D (2011) Agriculture: beyond food versus fuel. Nature 474:6-8
3. Leonowicz A, Cho N, Luterek J, Wilkolazka A, Wojtas-Wasilewska M, Matuszewska A, Hofrichter M, Wesenberg D, Rogalski J (2001) Fungal laccase: properties and activity on lignin. J Basic Microbiol 41:185-227
4. Fava F, Totaro G, Diels L, Reis M, Duarte J, Carioca OB, Poggi-Varaldo HM, Ferreira BS (2015) Biowaste biorefinery in Europe: opportunities and research & development needs. N Biotechnol 32:100-108
5. Doherty WOS, Mousavioun P, Fellows CM (2011) Value-adding to cellulosic ethanol: lignin polymers. Ind Crops Prod 33:259-276
6. Perlack R, Wright L, Turhollow A (2005) Biomass as feedstock for a bioenergy and bioproducts industry: the technical feasibility of a billion-ton annual supply. US Dep. Energy
7. Himmel M, Ding S, Johnson D (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804-807
8. Wyman CE, Dale BE, Elander RT, Holtzapple M, Ladisch MR, Lee YY (2005) Coordinated development of leading biomass pretreatment technologies. Bioresour Technol 96:1959-1966
9. Zhang YHP (2011) What is vital (and not vital) to advance economically-competitive biofuels production. Process Biochem 46:2091-2110
10. Yang B, Wyman CE (2008) Pretreatment: the key to unlocking low-cost cellulosic ethanol. Biofuels Bioprod Biorefining 2:26-40
11. Fischer R, Ostafe R, Twyman R (2013) Cellulases from insects. Adv Biochem Eng Biotechnol 136:51-64
12. Ke J, Laskar DD, Gao D, Chen S (2012) Advanced biorefinery in lower termite-effect of combined pretreatment during the chewing process. Biotechnol Biofuels 5:11
13. Zakzeski J, Bruijnincx PC, Jongerius AL, Weckhuysen BM (2009) The catalytic valorization of lignin for the production of renewable chemicals. Chem Rev 110:3552-3599
14. Chandra RP, Bura R, Mabee WE, Berlin A, Pan X, Saddler JN (2007) Substrate pretreatment: the key to effective enzymatic hydrolysis of lignocellulosics? In: Olsson L (ed) Biofuels. Springer, Berlin, Heidelberg, pp 67-93
15. Cullen D (1997) Recent advances on the molecular genetics of ligninolytic fungi. J Biotechnol 53:273-289
16. Call HP, Mücke I (1997) History, overview and applications of mediated lignolytic systems, especially laccase-mediator-systems (Lignozym(R)-process). J Biotechnol 53:163-202
17. Argyropoulos D, Menachem S (1997) Lignin. Adv Biochem Eng Biotechnol 57:127-158
18. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519-546
19. Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895-905
20. Lewis NG, Yamamoto E (1990) Lignin - occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41:455-496
21. Chakar FS, Ragauskas AJ (2004) Review of current and future softwood kraft lignin process chemistry. Ind Crops Prod 20:131-141
22. Demirbaş A (2001) Relationships between lignin contents and heating values of biomass. Energy Convers Manag 42:183-188
23. Azadi P, Inderwildi OR, Farnood R, King DA (2013) Liquid fuels, hydrogen and chemicals from lignin: a critical review. Renew Sustain Energy Rev 21:506-523
24. Yoshida H (1883) LXIII. Chemistry of lacquer (Urushi). Part I. Communication from the Chemical Society of Tokio. J Chem Soc Trans 43:472
25. Giardina P, Faraco V, Pezzella C, Piscitelli A, Vanhulle S, Sannia G (2010) Laccases: a never-ending story. Cell Mol Life Sci 67:369-385
26. Dwivedi UN, Singh P, Pandey VP, Kumar A (2011) Structure-function relationship among bacterial, fungal and plant laccases. J Mol Catal B Enzym 68:117-128
27. Dashtban M, Schraft H, Syed TA, Qin W (2010) Fungal biodegradation and enzymatic modification of lignin. Int J Biochem Mol Biol 1:36-50
28. 2O by the multicopper oxidases. Dalton Trans 9226:3921-3932
29. Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19-26
30. Yaropolov A, Skorobogatko O, Vartanov S, Varfolomeyev S (1994) Laccase - properties, catalytic mechanism and applicability. Appl Biochem Biotechnol 49:257-280
31. Shleev S, Reimann CT, Serezhenkov V, Burbaev D, Yaropolov AI, Gorton L, Ruzgas T (2006) Autoreduction and aggregation of fungal laccase in solution phase: possible correlation with a resting form of laccase. Biochimie 88:1275-1285
32. 2O at the trinuclear copper cluster active site in native laccase. J Am Chem Soc 124:6180-6193
33. Morozova O, Shumakovich G, Gorbacheva M, Shleev S, Yaropolov A (2007) "Blue" laccases. Biochem 72:1136-1150
34. 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
35. Leontievsky A, Myasoedova N, Baskunov B, Pozdnyakova N, Vares T, Kalkkinen N, Hatakka A, Golovleva L (1999) Reactions of blue and yellow fungal laccases with lignin model compounds. Biochem 64:1150-1156
36. Pozdnyakova N, Rodakiewicz-Nowak J, Turkovskaya O (2004) Catalytic properties of yellow laccase from Pleurotus ostreatus D1. J Mol Catal B Enzym 30:19-24
37. Baldrian P (2006) Fungal laccases - occurrence and properties. FEMS Microbiol Rev 30:215-242
38. Maijala P, Mattinen M-L, Nousiainen P, Kontro J, Asikkala J, Sipilä J, Viikari L (2012) Action of fungal laccases on lignin model compounds in organic solvents. J Mol Catal B Enzym 76:59-67
39. Rodakiewicz-Nowak J, Haber J, Pozdnyakova N, Leontievsky A, Golovleva LA (1999) Effect of ethanol on enzymatic activity of fungal laccases. Biosci Rep 19:589-600
40. Rodakiewicz-Nowak J, Jarosz-Wilkołazka A (2007) Catalytic activity of Cerrena unicolor laccase in aqueous solutions of water-miscible organic solvents - experimental and numerical description. J Mol Catal B Enzym 44:53-59
41. Cantarella G, d'Acunzo F, Galli C (2003) Determination of laccase activity in mixed solvents: comparison between two chromogens in a spectrophotometric assay. Biotechnol Bioeng 82:395-398
42. d'Acunzo F, Barreca AM, Galli C (2004) Determination of the activity of laccase, and mediated oxidation of a lignin model compound, in aqueous-organic mixed solvents. J Mol Catal B Enzym 31:25-30
43. Barreca AM, Fabbrini M, Galli C, Gentili P, Ljunggren S (2003) Laccase/mediated oxidation of a lignin model for improved delignification procedures. J Mol Catal B Enzym 26:105-110
44. Fiţigàu I, Peter F, Boeriu C (2013) Oxidative polymerization of lignins by laccase in water-acetone mixture. Acta Biochim Pol 60:817-822
45. Rehmann L, Ivanova E, Ferguson JL, Gunaratne HQN, Seddon KR, Stephens GM (2012) Measuring the effect of ionic liquids on laccase activity using a simple, parallel method. Green Chem 14:725-733
46. Harwardt N, Stripling N, Roth S, Liu H, Schwaneberg U, Spiess AC (2014) Effects of ionic liquids on the reaction kinetics of a laccase-mediator system. RSC Adv 4:17097-17104
47. Liu H, Zhu L, Bocola M, Chen N, Spiess AC, Schwaneberg U (2013) Directed laccase evolution for improved ionic liquid resistance. Green Chem 15:1348-1355
48. Crestini C, Argyropoulos DS (1998) The early oxidative biodegradation steps of residual kraft lignin models with laccase. Bioorg Med Chem 6:2161-2169
49. Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates: an expanded role for laccase in lignin biodegradation. FEBS Lett 267:99-102
50. Shiraishi T, Sannami Y, Kamitakahara H, Takano T (2013) Comparison of a series of laccase mediators in the electro-oxidation reactions of non-phenolic lignin model compounds. Electrochim Acta 106:440-446
51. 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
52. Xu F, Kulys J, Duke K (2000) Redox chemistry in laccase-catalyzed oxidation of N-hydroxy compounds. Appl Environ Microbiol 66:1-6
53. Fabbrini M, Galli C, Gentili P (2002) Comparing the catalytic efficiency of some mediators of laccase. J Mol Catal B Enzym 16:231-240
54. Fabbrini M, Galli C, Gentili P (2002) Radical or electron-transfer mechanism of oxidation with some laccase/mediator systems. J Mol Catal B Enzym 18:169-171
55. Galli C, Gentili P (2004) Chemical messengers: mediated oxidations with the enzyme laccase. J Phys Org Chem 17:973-977
56. Baiocco P, Barreca AM, Fabbrini M, Galli C, Gentili P (2003) Promoting laccase activity towards non-phenolic substrates: a mechanistic investigation with some laccase-mediator systems. Org Biomol Chem 1:191-197
57. Astolfi P, Brandi P, Galli C, Gentili P (2005) New mediators for the enzyme laccase: mechanistic features and selectivity in the oxidation of non-phenolic substrates. New J Chem 29:1308-1317
58. Fabbrini M, Galli C, Gentili P, Macchitella D (2001) An oxidation of alcohols by oxygen with the enzyme laccase and mediation by TEMPO. Tetrahedron Lett 42:7551-7553
59. Galli C, Gentili P, Lanzalunga O, Lucarini M, Pedulli GF (2004) Spectrophotometric, EPR and kinetic characterisation of the > N-O center dot radical from 1-hydroxybenzotriazole, a key reactive species in mediated enzymatic oxidations. Chem Commun (20):2356-2357
60. Arends IWCE, Li Y-X, Ausan R, Sheldon RA (2006) Comparison of TEMPO and its derivatives as mediators in laccase catalysed oxidation of alcohols. Tetrahedron 62:6659-6665
61. Shin W, Cho H, Cho N (2006) Screening of new mediators for lignin degradation based on their electrochemical properties and interactions with fungal laccase. J Korea TAPPI 38:5
62. Soares GMB, de Amorim MTP, Costa-Ferreira M (2001) Use of laccase together with redox mediators to decolourize Remazol Brilliant Blue R. J Biotechnol 89:123-129
63. Rehmann L, Ivanova E, Gunaratne HQN, Seddon KR, Stephens G, Gunaratne N (2013) Enhanced laccase stability through mediator partitioning into hydrophobic ionic liquids. Green Chem 16:1462-1469
64. Bendl RF, Kandel JM, Amodeo KD, Ryder AM, Woolridge EM (2008) Characterization of the oxidative inactivation of xylanase by laccase and a redox mediator. Enzyme Microb Technol 43:149-156
65. 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
66. Li K, Helm RF, Eriksson KL (1998) Mechanistic studies of the oxidation of a non-phenolic lignin model compound by the laccase/1-hydroxybenzotriazole redox system. Biotechnol Appl Biochem 27:239-243
67. Matsumura E, Yamamotoa E, Numataa A, Kawanoa T, Shin T, Murao S (1986) Structures of the laccase-catalyzed oxidation products of hydroxybenzoic acids in the presence of ABTS [2,2′-azino-di-(3-ethylbenzothiazoline-6-sulfonic acid)]. Agric Biol Chem 50:1355-1357
68. Rittstieg K, Suurnakki A, Suortti T, Kruus K, Guebitz G, Buchert J (2002) Investigations on the laccase-catalyzed polymerization of lignin model compounds using size-exclusion HPLC. Enzyme Microb Technol 31:403-410
69. Palonen H, Viikari L (2004) Role of oxidative enzymatic treatments on enzymatic hydrolysis of softwood. Biotechnol Bioeng 86:550-557
70. Eggert C, Temp U, Dean JFDD, Eriksson K-EEL (1996) A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase. FEBS Lett 391:144-148
71. Canas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28:694-705
72. Kawai S, Umezawa T, Higuchi T (1989) Oxidation of methoxylated benzyl alcohols by laccase of Coriolus versicolor in the presence of syringaldehyde. Wood Res 76:10-16
73. D'Acunzo F, Galli C (2003) First evidence of catalytic mediation by phenolic compounds in the laccase-induced oxidation of lignin models. Eur J Biochem 270:3634-3640
74. Calcaterra A, Galli C, Gentili P (2008) Phenolic compounds as likely natural mediators of laccase: a mechanistic assessment. J Mol Catal B Enzym 51:118-120
75. D'Acunzo F, Galli C, Gentili P, Sergi F (2006) Mechanistic and steric issues in the oxidation of phenolic and non-phenolic compounds by laccase or laccase-mediator systems. The case of bifunctional substrates. New J Chem 30:583
76. Martorana A, Sorace L, Boer H, Vazquez-Duhalt R, Basosi R, Baratto MC (2013) A spectroscopic characterization of a phenolic natural mediator in the laccase biocatalytic reaction. J Mol Catal B Enzym 97:203-208
77. Camarero S, Ibarra D, Martinez MJ, Martinez AT (2005) Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl Environ Microbiol 71:1775-1784
78. Cho NS, Shin W, Jeong SW, Leonowicz A (2004) Degradation of lignosulfonate by fungal laccase with low molecular mediators. Bull Korean Chem Soc 25:1551-1554
79. Nousiainen P, Maijala P, Hatakka A, Martínez AT, Sipilä J (2009) Syringyl-type simple plant phenolics as mediating oxidants in laccase catalyzed degradation of lignocellulosic materials: model compound studies. Holzforschung 63:699-704
80. Rico A, Rencoret J, del Rio J, Martinez A, Gutierrez A (2014) Pretreatment with laccase and a phenolic mediator degrades lignin and enhances saccharification of Eucalyptus feedstock. Biotechnol Biofuels 7:6
81. Du X, Li J, Gellerstedt G, Rencoret J, Del Rio JC, Martinez AT, Gutierrez A (2013) Understanding pulp delignification by laccase-mediator systems through isolation and characterization of lignin-carbohydrate complexes. Biomacromolecules 14:3073-3080
82. Moilanen U, Kellock M, Várnai A, Andberg M, Viikari L (2014) Mechanisms of laccase-mediator treatments improving the enzymatic hydrolysis of pre-treated spruce. Biotechnol Biofuels 7:3
83. Fillat A, Gallardo O, Vidal T, Pastor FIJ, Díaz P, Roncero MB (2012) Enzymatic grafting of natural phenols to flax fibres: development of antimicrobial properties. Carbohydr Polym 87:146-152
84. Vila C, Barneto AG, Fillat A, Vidal T, Ariza J (2011) Use of thermogravimetric analysis to monitor the effects of natural laccase mediators on flax pulp. Bioresour Technol 102:6554-6561
85. Torres-Duarte C, Roman R, Tinoco R, Vazquez-Duhalt R (2009) Halogenated pesticide transformation by a laccase-mediator system. Chemosphere 77:687-692
86. Kumar P, Barrett DM, Delwiche MJ, Stroeve P (2009) Methods for pretreatment of lignocellulosic biomass for efficient hydrolysis and biofuel production. Ind Eng Chem Res 48:3713-3729
87. Menon V, Rao M (2012) Trends in bioconversion of lignocellulose: biofuels, platform chemicals & biorefinery concept. Prog Energy Combust Sci 38:522-550
88. Zhu JY, Pan XJ (2010) Woody biomass pretreatment for cellulosic ethanol production: technology and energy consumption evaluation. Bioresour Technol 101:4992-5002
89. Viell J, Harwardt A, Seiler J, Marquardt W (2013) Is biomass fractionation by Organosolv-like processes economically viable? A conceptual design study. Bioresour Technol 150:89-97
90. Schmiedl D, Endisch S, Pindel E, Rückert D, Reinhardt S, Unkelbach U, Schweppe R (2012) Base catalyzed degradation of lignin for the generation of oxy-aromatic compounds - possibilities and challenges. Erdöl Erdgas Kohl 10:357-363
91. Gutiérrez A, Rencoret J, Cadena EM, Rico A, Barth D, del Río JC, Martínez ÁT (2012) Demonstration of laccase-based removal of lignin from wood and non-wood plant feedstocks. Bioresour Technol 119:114-122
92. Virk AP, Sharma P, Capalash N (2012) Use of laccase in pulp and paper industry. Biotechnol Prog 28:21-32
93. Widsten P, Kandelbauer A (2008) Laccase applications in the forest products industry: a review. Enzyme Microb Technol 42:293-307
94. Qiu W, Chen H (2012) Enhanced the enzymatic hydrolysis efficiency of wheat straw after combined steam explosion and laccase pretreatment. Bioresour Technol 118:8-12
95. Chakar FS, Ragauskas AJ (2004) Biobleaching chemistry of laccase-mediator systems on high-lignin-content kraft pulps. Can J Chem 82:344-352
96. Chen Q, Marshall MN, Geib SM, Tien M, Richard TL (2012) Effects of laccase on lignin depolymerization and enzymatic hydrolysis of ensiled corn stover. Bioresour Technol 117:186-192
97. Martin-Sampedro R, Capanema EA, Hoeger I, Villar JC, Rojas OJ (2011) Lignin changes after steam explosion and laccase-mediator treatment of eucalyptus wood chips. J Agric Food Chem 59:8761-8769
98. Pan X (2008) Role of functional groups in lignin inhibition of enzymatic hydrolysis of cellulose to glucose. J Biobased Mater Bioenergy 2:25-32
99. Moilanen U, Kellock M, Galkin S, Viikari L (2011) The laccase-catalyzed modification of lignin for enzymatic hydrolysis. Enzyme Microb Technol 49:492-498
100. Nakagame S, Chandra RP, Saddler JN (2010) The effect of isolated lignins, obtained from a range of pretreated lignocellulosic substrates, on enzymatic hydrolysis. Biotechnol Bioeng 105:871-879
101. Jetten JM, Van Den Dool R, Van Hartingsveldt W, Besemer AC (2000) Process for selective oxidation of cellulose. Patent WO2000050463 A1
102. Johanna B, Kristiina K, Liisa V (1999) Method for modification of cellulose. Patent WO1999023117
103. Besemer AC, De NAEJ (1995) Method for oxidising carbohydrates. Patent WO1995007303 A1
104. Chernoglazov V, Ermolova O, Klyosov A (1988) Adsorption of high-purity endo-1, 4-β-glucanases from Trichoderma reesei on components of lignocellulosic materials: cellulose, lignin, and xylan. Enzyme Microb Technol 10:503-507
105. Berlin A, Balakshin M, Gilkes N (2006) Inhibition of cellulase, xylanase and β-glucosidase activities by softwood lignin preparations. J Biotechnol 125:198-209
106. Converse AO, Ooshima H, Burns DS (1990) Kinetics of enzymatic hydrolysis of lignocellulosic materials based on surface area of cellulose accessible to enzyme and enzyme adsorption on lignin and cellulose. Appl Biochem Biotechnol 24-25:67-73
107. Rahikainen JL, Martin-Sampedro R, Heikkinen H, Rovio S, Marjamaa K, Tamminen T, Rojas OJ, Kruus K (2013) Inhibitory effect of lignin during cellulose bioconversion: the effect of lignin chemistry on non-productive enzyme adsorption. Bioresour Technol 133:270-278
108. Palonen H, Tjerneld F, Zacchi G, Tenkanen M (2004) Adsorption of Trichoderma reesei CBH I and EG II and their catalytic domains on steam pretreated softwood and isolated lignin. J Biotechnol 107:65-72
109. Heap L, Green A, Brown D, van Dongen B, Turner N (2014) Role of laccase as an enzymatic pretreatment method to improve lignocellulosic saccharification. Catal Sci Technol 4:2251-2259
110. Fillat U, Roncero MB (2009) Biobleaching of high quality pulps with laccase mediator system: influence of treatment time and oxygen supply. Biochem Eng J 44:193-198
111. Balakshin M, Capanema E, Chen C-L, Gratzl J, Kirkman A, Gracz H (2001) Biobleaching of pulp with dioxygen in the laccase-mediator system - reaction mechanisms for degradation of residual lignin. J Mol Catal B Enzym 13:1-16
112. Gierer J, Imsgard F, Norén I, Stilkerieg B, Christensen A, Schroll G (1977) Studies on the degradation of phenolic lignin units of the beta-aryl ether type with oxygen in alkaline media. Acta Chem Scand B 31:561-572
113. Kirk T, Farrell R (1987) Enzymatic "combustion": the microbial degradation of lignin. Annu Rev Microbiol 41:465-505
114. Law K (1950) Phenol oxidases in some wood-rotting fungi. Ann Bot 14:69-78
115. Fårhraeus G (1952) Formation of laccase by Polyporus versicolor in different culture media. Physiol Plant 5:284-291
116. Leonowicz A, Szklarz G, Wojtaś-Wasilewska M (1985) The effect of fungal laccase on fractionated lignosulphonates (Peritan Na). Phytochemistry 24:393-396
117. Ander P, Eriksson KE (1976) The importance of phenol oxidase activity in lignin degradation by the white-rot fungus Sporotrichum pulverulentum. Arch Microbiol 109:1-8
118. 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
119. Haars A, Hüttermann A (1980) Function of laccase in the white-rot fungus Fomes annosus. Arch Microbiol 237:233-237
120. Kirk T, Harkin J, Cowling E (1968) Degradation of the lignin model compound springgylglycol-β-guaiacyl ether by Polyporus versicolor and Stereum frustulatum. Biochim Biophys Acta 165:145-163
121. Van Vliet W (1954) The enzymatic oxidation of lignin. Biochim Biophys Acta 15:211-216
122. Gierer J, Opara A (1973) Studies on the enzymatic degradation of lignin. The action of peroxidase and laccase on monomeric and dimeric model compounds. Acta Chem Scand 27:2909-2922
123. Kirk TK (1971) Effects of microorganisms on lignin. Annu Rev Phytopathol 9:185-210
124. Srebotnik E, Hammel KE (2000) Degradation of nonphenolic lignin by the laccase/1-hydroxybenzotriazole system. J Biotechnol 81:179-188
125. Li KC, Xu F, Eriksson KEL (1999) Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl Environ Microbiol 65:2654-2660
126. 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
127. Rittstieg K, Suurnäkki A, Suortti T, Kruus K, Guebitz GM, Buchert J (2003) Polymerization of guaiacol and a phenolic β-O-4-substructure by Trametes hirsuta laccase in the presence of ABTS. Biotechnol Prog 19:1505-1509
128. 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
129. Castro A, Evtuguin D, Xavier A (2003) Degradation of biphenyl lignin model compounds by laccase of Trametes versicolor in the presence of 1-hydroxybenzotriazole and heteropolyanion. J Mol Catal B Enzym 22:13-20
130. Azarpira A, Ralph J, Lu F (2013) Catalytic alkaline oxidation of lignin and its model compounds: a pathway to aromatic biochemicals. BioEnergy Res 7:78-86
131. Xu C, Arancon RAD, Labidi J, Luque R (2014) Lignin depolymerisation strategies: towards valuable chemicals and fuels. Chem Soc Rev 43:7485-7500
132. West MA, Hickson AC, Mattinen ML, Lloyd-Jones G (2014) Evaluating lignins as enzyme substrates: insights and methodological recommendations from a study of laccase-catalyzed lignin polymerization. Bioresources 9:2782-2796
133. 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
134. Potthast A, Rosenau T, Koch H, Fischer K (1999) The reaction of phenolic model compounds in the laccase-mediator system (LMS) investigations by matrix assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF-MS). Holzforschung 53:175-180
135. Hernández Fernaud JRR, Carnicero A, Perestelo F, Hernández Cutuli M, Arias E, Falcón MA (2006) Upgrading of an industrial lignin by using laccase produced by Fusarium proliferatum and different laccase-mediator systems. Enzyme Microb Technol 38:40-48
136. Shleev S, Persson P, Shumakovich G, Mazhugo Y, Yaropolov A, Ruzgas T, Gorton L (2006) Interaction of fungal laccases and laccase-mediator systems with lignin. Enzyme Microb Technol 39:841-847
137. Munk L, Sitarz A, Kalyani D (2015) Can laccases catalyze bond cleavage in lignin? Biotechnol Adv. doi: 10.1016/j.biotechadv.2014.12.008
138. Mita N, Tawaki S, Uyama H, Kobayashi S (2003) Laccase-catalyzed oxidative polymerization of phenols. Macromol Biosci 3:253-257
139. Aktas N, Tanyolaç A (2003) Kinetics of laccase-catalyzed oxidative polymerization of catechol. J Mol Catal B Enzym 22:61-69
140. Ikeda R, Sugihara J, Uyama H, Kobayashi S (1996) Enzymatic oxidative polymerization of 2,6-dimethylphenol. Macromolecules 29:8702-8705
141. Ikeda R, Uyama H, Kobayashi S (1996) Novel synthetic pathway to a poly(phenylene oxide). Laccase-catalyzed oxidative polymerization of syringic acid. Macromolecules 29:3053-3054
142. Sun X, Bai R, Zhang Y, Wang Q, Fan X (2013) Laccase-catalyzed oxidative polymerization of phenolic compounds. Appl Biochem Biotechnol 171:1673-1680
143. Youn H, Hah Y, Kang S (1995) Role of laccase in lignin degradation by white-rot fungi. FEMS Microbiol Lett 132:183-188
144. Majumdar S, Lukk T, Solbiati J, Bauer S (2014) The roles of small laccases from Streptomyces in lignin degradation. Biochemistry 53:4047-4058
145. Arca-Ramos A, Eibes G, Moreira M (2012) Surfactant-assisted two phase partitioning bioreactors for laccase-catalyzed degradation of anthracene. Process Biochem 47:1115-1121
146. Arca-Ramos A, Eibes G, Moreira MT (2014) Vegetable oils as NAPLs in two phase partitioning bioreactors for the degradation of anthracene by laccase. Chem Eng J 240:281-289
147. Mustafa R, Muniglia L, Rovel B, Girardin M (2005) Phenolic colorants obtained by enzymatic synthesis using a fungal laccase in a hydro-organic biphasic system. Food Res Int 38:995-1000
148. Lee SH, Doherty TV, Linhardt RJ, Dordick JS (2009) Ionic liquid-mediated selective extraction of lignin from wood leading to enhanced enzymatic cellulose hydrolysis. Biotechnol Bioeng 102:1368-1376
149. Zhou G-P, Zhang Y, Huang X-R, Shi C-H, Liu W-F, Li Y-Z, Qu Y-B, Gao P-J (2008) Catalytic activities of fungal oxidases in hydrophobic ionic liquid 1-butyl-3-methylimidazolium hexafluorophosphate-based microemulsion. Colloids Surf B Biointerfaces 66:146-149
150. Xue L, Qiu H, Li Y, Lu L, Huang X, Qu Y (2011) A novel water-in-ionic liquid microemulsion and its interfacial effect on the activity of laccase. Colloids Surf B Biointerfaces 82:432-437
151. Alberti BN, Klibanov AM (1982) Preparative production of hydroquinone from benzoquinone catalysed by immobilized d-glucose oxidase. Enzyme Microb Technol 4:47-49
152. Green T (1977) Significance of glucose oxidase in lignin degradation. Nature 268:78-80
153. Szklarz G, Leonowicz A (1986) Cooperation between fungal laccase and glucose oxidase in the degradation of lignin derivatives. Phytochemistry 25:2537-2539
154. Leonowicz A, Rogalski J, Jaszek M, Luterek J, Wojtas-Wasilewska M, Malarczyk E, Ginalska G, Fink-Boots M, Cho N-S (1999) Cooperation of fungal laccase and glucose 1-oxidase in transformation of Björkman lignin and some phenolic compounds. Holzforschung 53:376-380
155. Marzullo L, Cannio R, Giardina P (1995) Veratryl alcohol oxidase from Pleurotus ostreatus participates in lignin biodegradation and prevents polymerization of laccase-oxidized substrates. J Biol Chem 270:3823-3827
156. Westermark U, Eriksson K (1974) Cellobiose: quinone oxidoreductase, a new wood-degrading enzyme from white-rot fungi. Scand B Acta Chem 28:209-214
157. Ander P, Mishra C, Farrell RL, Eriksson K-EL (1990) Redox reactions in lignin degradation: interactions between laccase, different peroxidases and cellobiose: quinone oxidoreductase. J Biotechnol 13:189-198
158. Eriksson K, Habu N, Samejima M (1993) Recent advances in fungal cellobiose oxidoreductases. Enzyme Microb Technol 15:1002-1008
159. Henriksson G, Johansson G, Pettersson G (2000) A critical review of cellobiose dehydrogenases. J Biotechnol 78:93-113
160. Picart P, Müller C, Mottweiler J, Wiermann L, Bol C, Domingues de Maria P, Schallmey A (2014) From gene towards selective biomass valorization: bacterial β-etherases with catalytic activity on lignin-like polymers. CemSusChem 7:3164-3171
161. Reiter J, Strittmatter H, Wiemann L, Schieder D, Sieber V (2013) Enzymatic cleavage of lignin β-O-4 aryl ether bonds via net internal hydrogen transfer. Green Chem 15:1373
162. Lin S, Dence C (1992) Methods in lignin chemistry. Springer, Berlin, Heidelberg
163. Baumberger S, Abaecherli A, Fasching M, Gellerstedt G, Gosselink R, Hortling B, Li J, Saake B, de Jong E (2007) Molar mass determination of lignins by size-exclusion chromatography: towards standardisation of the method. Holzforschung 61:459-468
164. Contreras S, Gaspar AR, Guerra A, Lucia LA, Argyropoulos DS (2008) Propensity of lignin to associate: light scattering photometry study with native lignins. Biomacromolecules 9:3362-3369
165. Cathala B, Saake B, Faix O, Monties B (2003) Association behaviour of lignins and lignin model compounds studied by multidetector size-exclusion chromatography. J Chromatogr A 1020:229-239
166. Guerra A, Gaspar AR, Contreras S, Lucia LA, Crestini C, Argyropoulos DS (2007) On the propensity of lignin to associate: a size exclusion chromatography study with lignin derivatives isolated from different plant species. Phytochemistry 68:2570-2583
167. Connors WJ, Sarkanen S, McCarthy JL (1980) Gel chromatography and association complexes of lignin. Holzforschung 34:80-85
168. Yuan T-Q, Sun S-N, Xu F, Sun R-C (2011) Characterization of lignin structures and lignin-carbohydrate complex (LCC) linkages by quantitative 13C and 2D HSQC NMR spectroscopy. J Agric Food Chem 59:10604-10614
169. Sette M, Wechselberger R, Crestini C (2011) Elucidation of lignin structure by quantitative 2D NMR. Chem A Eur J 17:9529-9535
170. Sette M, Lange H, Crestini C (2013) Quantitative HSQC analyses of lignin: a practical comparison. Comput Struct Biotechnol J 6:1-7
171. Rencoret J, Marques G, Gutierrez A, Nieto L, Santos JI, Jimenez-Barbero J, Martinez AT, del Rio JC (2009) HSQC-NMR analysis of lignin in woody (Eucalyptus globulus and Picea abies) and non-woody (Agave sisalana) ball-milled plant materials at the gel state 10(th) EWLP, Stockholm, Sweden, August 25-28, 2008. Holzforschung 63:691-698
172. Capanema EA, Balakshin MY, Kadla JF (2005) Quantitative characterization of a hardwood milled wood lignin by nuclear magnetic resonance spectroscopy. J Agric Food Chem 53:9639-9649
173. Chandel AK, da Silva SS, Singh OV (2012) Detoxification of lignocellulose hydrolysates: biochemical and metabolic engineering toward white biotechnology. BioEnergy Res 6:388-401
174. Klinke HB, Thomsen AB, Ahring BK (2004) Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol 66:10-26
175. Ximenes E, Kim Y, Mosier N, Dien B, Ladisch M (2011) Deactivation of cellulases by phenols. Enzyme Microb Technol 48:54-60
176. Ximenes E, Kim Y, Mosier N, Dien B, Ladisch M (2010) Inhibition of cellulases by phenols. Enzyme Microb Technol 46:170-176
177. Kim Y, Ximenes E, Mosier NS, Ladisch MR (2011) Soluble inhibitors/deactivators of cellulase enzymes from lignocellulosic biomass. Enzyme Microb Technol 48:408-415
178. Tejirian A, Xu F (2011) Inhibition of enzymatic cellulolysis by phenolic compounds. Enzyme Microb Technol 48:239-247
179. Palmqvist E, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25-33
180. Heipieper HJ, Weber FJ, Sikkema J, Keweloh H, de Bont JA (1994) Mechanisms of resistance of whole cells to toxic organic solvents. Trends Biotechnol 12:409-415
181. Mussatto SI, Roberto IC (2004) Alternatives for detoxification of diluted-acid lignocellulosic hydrolyzates for use in fermentative processes: a review. Bioresour Technol 93:1-10
182. Olsson L, Hahn-Hägerdal B (1996) Fermentation of lignocellulosic hydrolysates for ethanol production. Enzyme Microb Technol 18:312-331
183. Palmqvist E, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates. I: inhibition and detoxification. Bioresour Technol 74:17-24
184. Jönsson L, Palmqvist E (1998) Detoxification of wood hydrolysates with laccase and peroxidase from the white-rot fungus Trametes versicolor. Appl Microbiol 49:691-697
185. Jurado M, Prieto A, Martínez-Alcalá A, Martínez AT, Martínez MJ (2009) Laccase detoxification of steam-exploded wheat straw for second generation bioethanol. Bioresour Technol 100:6378-6384
186. Larsson S, Reimann A (1999) Comparison of different methods for the detoxification of lignocellulose hydrolyzates of spruce. Appl Biochem Biotechnol 77:91-103
187. Martín C, Galbe M (2002) Ethanol production from enzymatic hydrolysates of sugarcane bagasse using recombinant xylose-utilising Saccharomyces cerevisiae. Enzyme Microb Technol 31:274-282
188. Chandel AK, Kapoor RK, Singh A, Kuhad RC (2007) Detoxification of sugarcane bagasse hydrolysate improves ethanol production by Candida shehatae NCIM 3501. Bioresour Technol 98:1947-1950
189. Moreno A, Ibarra D (2012) Different laccase detoxification strategies for ethanol production from lignocellulosic biomass by the thermotolerant yeast Kluyveromyces marxianus CECT. Bioresour Technol 106:101-109
190. Moreno AD, Tomás-Pejó E, Ibarra D, Ballesteros M, Olsson L (2013) In situ laccase treatment enhances the fermentability of steam-exploded wheat straw in SSCF processes at high dry matter consistencies. Bioresour Technol 143:337-343
191. Guo F, Shi W, Sun W, Li X, Wang F, Zhao J, Qu Y (2014) Differences in the adsorption of enzymes onto lignins from diverse types of lignocellulosic biomass and the underlying mechanism. Biotechnol Biofuels 7:38
192. Lee K-M, Kalyani D, Tiwari MK, Kim T-S, Dhiman SS, Lee J-K, Kim I-W (2012) Enhanced enzymatic hydrolysis of rice straw by removal of phenolic compounds using a novel laccase from yeast Yarrowia lipolytica. Bioresour Technol 123:636-645
193. Ludwig D, Amann M, Hirth T, Rupp S, Zibek S (2013) Development and optimization of single and combined detoxification processes to improve the fermentability of lignocellulose hydrolyzates. Bioresour Technol 133:455-461
194. Jäger G, Büchs J (2012) Biocatalytic conversion of lignocellulose to platform chemicals. Biotechnol J. doi: 10.1002/biot.201200033
195. Klement T, Büchs J (2012) Itaconic acid - a biotechnological process in change. Bioresour Technol 135:422-431
196. Palmqvist E, Hahn-Hägerdal B, Galbe M, Zacchi G (1996) The effect of water-soluble inhibitors from steam-pretreated willow on enzymatic hydrolysis and ethanol fermentation. Enzyme Microb Technol 19:470-476
197. Kudanga T, Le Roes-Hill M (2014) Laccase applications in biofuels production: current status and future prospects. Appl Microbiol Biotechnol 98:6525-6542
198. Morozova O, Shumakovich G, Shleev S, Yaropolov Y (2007) Laccase-mediator systems and their applications: a review. Appl Biochem Microbiol 43:523-535
199. Riva S (2006) Laccases: blue enzymes for green chemistry. Trends Biotechnol 24:219-226
200. Martín-Sampedro R, Eugenio ME, Carbajo JM, Villar JC (2011) Combination of steam explosion and laccase-mediator treatments prior to Eucalyptus globulus kraft pulping. Bioresour Technol 102:7183-7189
201. Kuila A, Mukhopadhyay M, Tuli DK, Banerjee R (2011) Accessibility of enzymatically delignified bambusa bambos for efficient hydrolysis at minimum cellulase loading: an optimization study. Enzyme Res 2011:1-8
202. Nugroho Prasetyo E, Kudanga T, Østergaard L, Rencoret J, Gutiérrez A, del Río JC, Ignacio Santos J, Nieto L, Jiménez-Barbero J, Martínez AT, Li J, Gellerstedt G, Lepifre S, Silva C, Kim SY, Cavaco-Paulo A, Seljebakken Klausen B, Lutnaes BF, Nyanhongo GS, Guebitz GM (2010) Polymerization of lignosulfonates by the laccase-HBT (1-hydroxybenzotriazole) system improves dispersibility. Bioresour Technol 101:5054-5062
203. Crestini C, Melone F, Saladino R (2011) Novel multienzyme oxidative biocatalyst for lignin bioprocessing. Bioorg Med Chem 19:5071-5078
204. van de Pas D, Hickson A, Donaldson L (2011) Characterization of fractionated lignins polymerized by fungal laccases. BioResources 6:1105-1121
205. Kalyani D, Dhiman SS, Kim H, Jeya M, Kim I-W, Lee J-K (2012) Characterization of a novel laccase from the isolated Coltricia perennis and its application to detoxification of biomass. Process Biochem 47:671-678
206. Kolb M, Sieber V, Amann M, Faulstich M, Schieder D (2012) Removal of monomer delignification products by laccase from Trametes versicolor. Bioresour Technol 104:298-304
207. Moreno AD, Ibarra D, Ballesteros I, González A, Ballesteros M (2013) Comparing cell viability and ethanol fermentation of the thermotolerant yeast Kluyveromyces marxianus and Saccharomyces cerevisiae on steam-exploded biomass treated with laccase. Bioresour Technol 135:239-245
208. Van Parijs FRD, Morreel K, Ralph J, Boerjan W, Merks RMH (2010) Modeling lignin polymerization. I. Simulation model of dehydrogenation polymers. Plant Physiol 153:1332-1344
209. 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