Abstract
Laccases have low redox potentials limiting their environmental and industrial applications. The use of laccase mediators has proven to be an effective approach for overcoming the low redox potentials. However, knowledge about the role played by the mediator cocktails in such a laccase-mediator system (LMS) is scarce. Here, we assembled different dual-agent mediator cocktails containing 2,2′-azino-bis-(3-ethylbenzothiazoline-6-sulfonate) (ABTS), vanillin, and/or acetovanillone, and compared their mediating capabilities with those of each individual mediator alone in oxidation of pentachlorophenol (PCP) by Ganoderma lucidum laccase. Cocktails containing ABTS and either vanillin or acetovanillone strongly promoted PCP removal compared to the use of each mediator alone. The removal enhancement was correlated with mediator molar ratios of the cocktails and incubation times. Analysis of the kinetic constants for each mediator compound showed that G. lucidum laccase was very prone to react with ABTS rather than vanillin and acetovanillone in the cocktails. Moreover, the presence of the ABTS radical (ABTS+•) and vanillin or acetovanillone significantly enhanced PCP removal concomitant with electron transfer from vanillin or acetovanillone to ABTS+•. These results strongly suggest that vanillin and acetovanillone mediate the reaction between ABTS and PCP via multiple sequential electron transfers among laccase and its mediators.
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Baiocco PA, Barreca AM, Fabbrini M, Galli C, Gentili P (2003) Promoting laccase activity towards non-phenolic substrates: a mechanistic investigation with some laccase-mediator system. Org Biomol Chem 1:191–197
Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbiol Rev 30:215–242
Bollag J-M, Shuttleworth KL, Anderson DH (1988) Laccase-mediated detoxification of phenolic compounds. Appl Environ Microbiol 54:3086–3091
Bourbonnais R, Paice MG (1990) Oxidation of nonphenolic substrates—an expanded role for laccase in lignin degradation. FEBS Lett 267:99–102
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
Camarero S, Ibarra D, Martínez MJ, Martínez AT (2005) Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl Environ Microbiol 71:1775–1784
Cañas A, Alcalde M, Plou F, Martínez MJ, Martínez AT, Camarero S (2007) Transformation of polycyclic aromatic hydrocarbons by laccase is strongly enhanced by phenolic compounds present in soil. Environ Sci Technol 41:2964–2971
Claus H (2003) Laccases and their occurrence in prokaryotes. Arch Microbiol 179:145–150
Collins PJ, Kotterman MJ, Field JA, Dobson ADW (1996) Oxidation of anthracene and benzo[a]pyrene by laccases from Trametes versicolor. Appl Environ Microbiol 62:4563–4567
David CB, Phillip MF, Michael AP (2000) Oxidation of carbazole, N-ethylcarbazole, fluorene, and dibenzothiophene by the laccase of Coriolopsis gallica. Appl Microbial Biotechnol 22:1119–1125
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
Fernández-Sánchez C, Tzanov T, Gübitz GM, Cavaco-Paulo A (2002) Voltammetric monitoring of laccase-catalyzed mediated reactions. Biochemistry 58:149–156
Gutiérrez A, Rencoret J, Ibarra D, Molina S, Camarero S, Romero J, Río JCD, Martínez AT (2007) Removal of lipophilic extractives from paper pulp by laccase and lignin-derived phenols as natural mediators. Environ Sci Technol 41:4124–4129
Holwerda RA, Wherland S, Gray HB (1976) Electron transfer reactions of copper proteins. Annu Rev Biophys Bioeng 5:363–396
Ikeda R, Uyama H, Kobayasi S (1996) Novel synthetic pathway to a poly(phenylene oxide). Laccase-catalyzed oxidative polymerization of syringic acid. Macromolecules 29:3053–3054
Jensen J (1996) Chlorophenols in the terrestrial environment. Rev Environ Contam Toxicol 146:25–51
Johannes C, Majcherczyk A (2000) Natural mediators in the oxidation of polycyclic aromatic hydrocarbons by laccase mediator systems. Appl Environ Microbiol 66:524–528
Keum YS, Li QX (2004) Fungal laccase-catalyzed degradation of hydroxy polychlorinated biphenyls. Chemosphere 56:23–30
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
Lundquist K, Kristersson P (1985) Exhaustive laccase-catalyzed oxidation of a lignin model compound (vanillyl glycol) produces methanol and polymeric quinoid products. Biochem J 229:277–279
Majchereczyk 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
Marzullo L, Cannio R, Giardina P, Santini MT, Sannia G (1995) Veratryl alcohol oxidase from Pleurotus ostreatus participates in lignin biodegradation and prevents polymerization of laccase-oxidized substrates. J Biol Chem 270:3823–3827
Mayer AM, Staples RC (2002) Laccase: new function for an old enzyme. Phytochemistry 60:551–565
Mikolasch A, Hammer E, Jonas U, Popowski K, Stielow A, Schauer F (2002) Synthesis of 3-(3,4-dihydroxyphenyl)-propionic acid derivatives by N-coupling of amines using laccase. Tetrahedron 58:7589–7593
Mita N, Tawaki S-I, Uyama H, Kobayasi S (2003) Laccase-catalyzed oxidative polymerization of phenols. Macromo Biosci 3:253–257
Muñoz C, Guillén F, Martínez MJ, Martínez AT (1997a) Induction and characterization of laccase in the ligninolytic fungus Pleurotus eryngii. Curr Microbiol 34:1–5
Muñoz C, Guillén F, Martínez MJ, Martínez AT (1997b) Laccase isoenzymes of Pleurotus eryngii: characterization, catalytic properties, and participation in activation of molecular oxygen and Mn2+ oxidation. Appl Environ Microbiol 63:2166–2174
Murugesan K, Arulmani M, Nam IH, Kim YM, Chang YS, Kalaichelvan PT (2006) Purification and characterization of laccase produced by a white rot fungus Pleurotus sajor-caju under submerged culture condition and its potential in decolorization of azo dyes. Appl Microbiol Biotechnol 72:939–946
Murugesan K, Nam IH, Kim YM, Chang YS (2007) Decolorization of reactive dyes by a thermostable laccase produced by Genoderma lucidum in solid state culture. Enzyme Microb Technol 40:1662–1672
Nicotra S, Cramarossa MR, Mucci A, Pagnoni UM, Riva S, Forti L (2004) Biotransformation of resveratrol: synthesis of trans-dehydrodimers catalyzed by laccases from Myceliophtora thermophyla and from Trametes pubescens. Tetrahedron 60:595–600
Paice MG, Bourbonnais R, Reid LD, Archibald FS, Jurasek L (1995) Oxidative bleaching enzymes: a review. J Pulp Paper Sci 21:J280–J284
Pylypenko O, Schlichting I (2004) Structure aspects of ligand binding to and electron transfer in bacterial and fungal P450S. Annu Rev Biochem 73:991–1018
Reid ID, Paice MG (1994) Biological bleaching of kraft pulps by white-rot fungi and their enzymes. FEMS Microbiol Rev 13:369–376
Riva S (2006) Laccases: blue enzymes for green chemistry. Trends Biotechnol 24:219–226
Roy-Arcand L, Archibald FS (1991) Direct dechlorination of chlorophenolic compounds by laccases from Trametes (Coriolus) versicolor. Enzyme Microb Technol 13:194–203
Santosh Kumar S, Priyadarsini KI, Sainis KB (2002) Free radical scavenging activity of vanillin and o-vanillin using 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical. Redox Rep 6:35–40
Tatiana D, Galina T, Vilhelmina J, Uldis V (2004) Characterization of the radical scavenging activity of lignin—natural antioxidants. Bioresour Technol 3:309–317
Ullah MA, Bedford CT, Evans CS (2000) Reactions of pentachlorophenol with laccase from Coriolus versicolor. Appl Microbiol Biotechnol 53:230–234
Wolfenden BS, Wilson RL (1982) Radical cations as reference chromogens in studies of one-electron transfer reactions: pulse radio analysis studies of 2,2′-azinobis-(3-ethlbenzthiazoline-b-sulfonate). J Chem Soc Perkin Trans II:805–812
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
Xu F, Kulys JJ, Duke K, Li KC, Krikstopaitis K, Deussen H-JW, Abbate E, Galinyte V, Schneider P (2000) Redox chemistry in laccase-catalyzed oxidation of N-hydroxy compounds. Appl Environ Microbiol 66:2052–2056
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This research was supported by Korea Ministry of Environment as “The GAIA project” and “The BK21 project”.
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Jeon, JR., Murugesan, K., Kim, YM. et al. Synergistic effect of laccase mediators on pentachlorophenol removal by Ganoderma lucidum laccase. Appl Microbiol Biotechnol 81, 783–790 (2008). https://doi.org/10.1007/s00253-008-1753-2
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DOI: https://doi.org/10.1007/s00253-008-1753-2