Abstract
Heme-containing peroxidases secreted by fungi are a fascinating group of biocatalysts with various ecological and biotechnological implications. For example, they are involved in the biodegradation of lignocelluloses and lignins and participate in the bioconversion of other diverse recalcitrant compounds as well as in the natural turnover of humic substances and organohalogens. The current review focuses on the most recently discovered and novel types of heme-dependent peroxidases, aromatic peroxygenases (APOs), and dye-decolorizing peroxidases (DyPs), which catalyze remarkable reactions such as peroxide-driven oxygen transfer and cleavage of anthraquinone derivatives, respectively, and represent own separate peroxidase superfamilies. Furthermore, several aspects of the “classic” fungal heme-containing peroxidases, i.e., lignin, manganese, and versatile peroxidases (LiP, MnP, and VP), phenol-oxidizing peroxidases as well as chloroperoxidase (CPO), are discussed against the background of recent scientific developments.
Similar content being viewed by others
Notes
Nomenclature Committee of the International Union of Biochemistry and Molecular Biology
A recent search in GenBank in February 2010 revealed more than 1,500 fungal nucleotide and 2,200 predicted fungal protein sequences annotated as “peroxidases.”
According to the Index fungorum (http://www.indexfungorum.org), the fungus belongs to the incertae sedis, i.e., it has an uncertain position within the Ascomycotina. Other authors classify C. fumago in the neighborhood of the mitosporic Capnodiaceae (Reynolds and Faull 2001).
In some respects, hypohalite formation can be also regarded as an oxygen transfer reaction.
In earlier publications, this enzyme was also referred to as Agrocybe aegerita peroxidase/peroxygenase (AaP), or haloperoxidase–peroxygenase (e.g., Ullrich et al. 2004; Ullrich and Hofrichter 2005; Hofrichter and Ullrich 2006; Kluge et al. 2007). Because of the discovery of more and more aromatic peroxygenases, they should be systematically abbreviated by the capital letter of the genus plus the first and second letter of the epitheton and the acronym APO (that stands for aromatic peroxygenase): for example, AaeAPO, aromatic peroxygenase of Agrocybe aegerita.
According to the Index fungorum (http://www.indexfungorum.org), the species is referred to as Mycetinis scorodonius named by Wilson and Desjardin (2005).
References
Alvarado B, Torres E (2009) Recents patents in the use of peroxidases. Recent Pat Biotechnol 3:88–102
Anh DH, Ullrich R, Benndorf D, Svatos A, Muck A, Hofrichter M (2007) The coprophilous mushroom Coprinus radians secretes a haloperoxidase that catalyzes aromatic peroxygenation. Appl Environ Microbiol 73:5477–5485
Aranda E, Kinne M, Kluge M, Ullrich R, Hofrichter M (2009) Conversion of dibenzothiophene by the mushrooms Agrocybe aegerita and Coprinellus radians and their extracellular peroxygenases. Appl Microbiol Biotechnol 82:1057–1066
Aranda E, Ullrich R, Hofrichter M (2010) Conversion of polycyclic aromatic hydrocarbons, methyl naphthalenes and dibenzofuran by two fungal peroxygenases. Biodegradation 21:267–281
Ayala M, Robledo NR, Lopez-Munguia A, Vazquez-Duhalt R (2000) Substrate specificity and ionization potential in chloroperoxidase-catalyzed oxidation of diesel fuel. Environ Sci Technol 34:2804–2809
Ayala M, Roman R, Vazquez-Duhalt R (2007) A catalytic approach to estimate the redox potential of heme-peroxidases. Biochem Biophys Res Commun 357:804–808
Ayala M, Pickard MA, Vazquez-Duhalt R (2008) Fungal enzymes for environmental purposes, a molecular biology challenge. J Mol Microbiol Biotechnol 15:172–180
Azevedo AM, Martins VC, Prazeres DM, Vojinovic V, Cabral JM, Fonseca LP (2003) Horseradish peroxidase: a valuable tool in biotechnology. Biotechnol Annu Rev 9:199–247
Baciocchi E, Bietti M, Gerini MF, Lanzalunga O (2002) The mediation of veratryl alcohol in oxidations promoted by lignin peroxidase: the lifetime of veratryl alcohol radical cation. Biochem Biophys Res Commun 293:832–835
Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbiol Rev 30:215–242
Banci L, Ciofi-Baffoni S, Tien M (1999) Lignin and Mn peroxidase-catalyzed oxidation of phenolic lignin oligomers. Biochemistry 38:3205–3210
Bengtson P, Bastviken D, de Boer W, Oberg G (2009) Possible role of reactive chlorine in microbial antagonism and organic matter chlorination in terrestrial environments. Environ Microbiol 11:1330–1339
Blanke SR, Yi S, Hager LP (1989) Development of semi-continuous and continuous flow bioreactors for the high level production of chloroperoxidase. Biotechnol Lett 11:769–774
Blodig W, Smith AT, Doyle WA, Piontek K (2001) Crystal structures of pristine and oxidatively processed lignin peroxidase expressed in Escherichia coli and of the W171F variant that eliminates the redox active tryptophan 171. Implications for the reaction mechanism. J Mol Biol 305:851–861
Bond AM, Fleming BD, Martin LL (2007) The electrochemistry of cytochrome P450. In: Sigel A, Sigel H, Sigel RKO (eds) Metal ions in life sciences, 1st edn. John Wiley & Sons Ltd, Chichester, pp 127–155
Borole AP, Davison BH (2007) Techno-economic analysis of biocatalytic processes for production of alkene epoxides. Appl Biochem Biotechnol 137–140:437–449
Bumpus JA (1989) Biodegradation of polycyclic hydrocarbons by Phanerochaete chrysosporium. Appl Environ Microbiol 55:154–158
Cai D, Tien M (1992) Kinetic studies on the formation and decomposition of compounds II and III. Reactions of lignin peroxidase with H2O2. J Biol Chem 267:11149–11155
Cartron ML, Mitchell SA, Woodhall MR, Andrews SC, Watson KA (2007) Preliminary X-ray diffraction analysis of YcdB from Escherichia coli: a novel haem-containing and Tat-secreted periplasmic protein with a potential role in iron transport. Acta Crystallogr F Struct Biol Cryst Commun 63:37–41
Casella L, Poli S, Gullotti M, Selvaggini C, Beringhelli T, Marchesini A (1994) The chloroperoxidase-catalyzed oxidation of phenols. Mechanism, selectivity, and characterization of enzyme-substrate complexes. Biochemistry 33:6377–6386
Chang HC, Holland RD, Bumpus JA, Churchwell MI, Doerge DR (1999) Inactivation of Coprinus cinereus peroxidase by 4-chloroaniline during turnover: comparison with horseradish peroxidase and bovine lactoperoxidase. Chemico-Biol Int 123:197–217
Chiang R, Rand-Meir T, Makino R, Hager LP (1976) Compound X. An intermediate in enzymatic halogenation. J Biol Chem 251:6340–6346
Choinowski T, Blodig W, Winterhalter KH, Piontek K (1999) The crystal structure of lignin peroxidase at 1.70 A resolution reveals a hydroxy group on the cβ of tryptophan 171: a novel radical site formed during the redox cycle. J Mol Biol 286:809–827
Conesa A, Punt PJ, van Luijk N, van den Hondel CA (2001) The secretion pathway in filamentous fungi: a biotechnological view. Fungal Genet Biol 33:155–171
Conesa A, Punt PJ, van den Hondel CA (2002) Fungal peroxidases: molecular aspects and applications. J Biotechnol 93:143–158
Cullen D (1997) Recent advances on the molecular genetics of ligninolytic fungi. J Biotechnol 53:273–289
Dai L, Klibanov AM (2000) Peroxidase-catalyzed asymmetric sulfoxidation in organic solvents versus in water. Biotechnol Bioeng 70:353–357
Dau AH (2008) Novel extracellular haloperoxidase-peroxygenases from the coprophilous fungi Coprinus radians and Coprinus verticillatus: production, purification and biochemical characterization. Ph.D. Thesis (dissertation), Unit of Environmental Biotechnology, International Graduate School of Zittau (Germany)
Dawson JH (1988) Probing structure-function relations in heme-containing oxygenases and peroxidases. Science 240:433–439
de Hoog HM, Nallani M, Cornelissen JJ, Rowan AE, Nolte RJ, Arends IW (2009) Biocatalytic oxidation by chloroperoxidase from Caldariomyces fumago in polymersome nanoreactors. Org Biomol Chem 7:4604–4610
Dingler C, Ladner W, Krei GA, Cooper BS, Hauer B (1996) Preparation of (R)-2-(4-hydroxyphenoxy)propionic acid by biotransformation. Pestic Sci 46:33–53
Doyle WA, Blodig W, Veitch NC, Piontek K, Smith AT (1998) Two substrate interaction sites in lignin peroxidase revealed by site-directed mutagenesis. Biochemistry 37:15097–15105
Dunford HB (1991) Horseradish peroxidase: structure and kinetic properties. In: Everse J, Everse KE, Grisham MB (eds) Peroxidases in chemistry and biology, 1st edn. CRC Press, Boca Raton, Ann Arbor, Boston, pp 1–24
Dunford HB (1999) Heme peroxidases, 1st edn. Wiley-VCH, New York
Everse J, Everse KE, Grisham MB (1991a) Peroxidases in chemistry and biology. 1st edn., vol. I, 1st edn. CRC Press, Boca Raton, Ann Arbor, Boston
Everse J, Everse KE, Grisham MB (1991b) Peroxidases in chemistry and biology. 1st edn., vol. II. CRC Press, Boca Raton, Ann Arbor, Boston
Faraco V, Piscitelli A, Sannia G, Giardina P (2007) Identification of a new member of the dye-decolorizing peroxidase family from Pleurotus ostreatus. World J Microbiol Biotechnol 23:889–893
Ferreira P, Hernández-Ortega A, Herguedas B, Martínez AT, Medina M (2009) Aryl-alcohol oxidase involved in lignin degradation: a mechanistic study based on steady and pre-steady state kinetics and primary and solvent isotope effects with two alcohol substrates. J Biol Chem 284:28840–28847
Fleischmann P, Zorn H (2008) Enzymic pathways for formation of carotenoid cleavage products. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids: natural functions, 1st edn. Birkhäuser, Basel, pp 341–366
Fleischmann A, Darsow M, Degtyarenko K, Fleischmann W, Boyce S, Axelsen KB, Bairoch A, Schomburg D, Tipton KF, Apweiler R (2004) IntEnz, the integrated relational enzyme database. Nucleic Acids Res 32:D434–D437
Fournier D, Halasz A, Spain J, Spanggord RJ, Bottaro JC, Hawari J (2004) Biodegradation of the hexahydro-1, 3, 5-trinitro-1, 3, 5-triazine ring cleavage product 4-nitro-2, 4-diazabutanal by Phanerochaete chrysosporium. Appl Environ Microbiol 70:1123–1128
Gazarian IG, Lagrimini LM (1996) Purification and unusual kinetic properties of a tobacco anionic peroxidase. Phytochemistry 41:1029–1034
Gazarian IG, Lagrimini LM (1998) Anaerobic stopped-flow studies of indole-3-acetic acid oxidation by dioxygen catalysed by horseradish C and anionic tobacco peroxidase at neutral pH: catalase effect. Biophys Chem 72:231–237
Gazarian IG, Lagrimini LM, Mellon FA, Naldrett MJ, Ashby GA, Thorneley RN (1998) Identification of skatolyl hydroperoxide and its role in the peroxidase-catalysed oxidation of indol-3-yl acetic acid. Biochem J 333(Pt1):223–232
Gedig T, Decker D, Scheibner K, Hofrichter M, Ullrich R, Kluge M (2008) Process for the preparation of optically active 1-arylalcohols using the haloperoxidase of Agrocybe aegerita. patent, WO/2008/028526
Geigert J, Lee TD, Dalietos DJ, Hirano DS, Neidleman SL (1986) Epoxidation of alkenes by chloroperoxidase catalysis. Biochem Biophys Res Commun 136:778–782
Gold MH, Youngs HL, Gelpke MD (2000) Manganese peroxidase. Met Ions Biol Syst 37:559–586
Gonzalez FJ (2005) Role of cytochromes P450 in chemical toxicity and oxidative stress: studies with CYP2E1. Mutat Res 569:101–110
Grey CE, Rundbäck F, Adlercreutz P (2008) Improved operational stability of chloroperoxidase through use of antioxidants. J Biotechnol 135:196–201
Hager LP, Morris DR, Brown FS, Eberwein H (1966) Chloroperoxidase. II. Utilization of halogen anions. J Biol Chem 241:1769–1777
Hammel KE, Cullen D (2008) Role of fungal peroxidases in biological ligninolysis. Curr Opin Plant Biol 11:349–355
Hammel KE, Moen MA (1991) Depolymerization of a synthetic lignin in vitro by lignin peroxidase. Enzyme Microb Technol 13:15–18
Hammel KE, Kalyanaraman B, Kirk TK (1986) Oxidation of polycyclic aromatic hydrocarbons and dibenzo[p]-dioxins by Phanerochaete chrysosporium ligninase. J Biol Chem 261:16948–16952
Hammel KE, Jensen KA Jr, Mozuch MD, Landucci LL, Tien M, Pease EA (1993) Ligninolysis by a purified lignin peroxidase. J Biol Chem 268:12274–12281
Hanano A, Burcklen M, Flenet M, Ivancich A, Louwagie M, Garin J, Blee E (2006) Plant seed peroxygenase is an original heme-oxygenase with an EF-hand calcium binding motif. J Biol Chem 281:33140–33151
Hatakka A (2001) Biodegradation of lignin. In: Hofrichter M, Steinbüchel A (eds) Biopolymers: lignin, humic substances and coal, 1st edn. Wiley-VCH, Weinheim, pp 129–180
Hatakka A, Hammel KE (2010) Fungal biodegradation of lignocelluloses. In: Hofrichter M (ed.) The Mycota, X, Industrial applications, 2nd edn. Springer, Berlin Heidelberg New York (in press)
Hatakka A, Lundell T, Hofrichter M, Maijala P (2003) Manganese peroxidase and its role in the degradation of wood lignin. In: Mansfield SD, Saddler JN (eds) Applications of enzymes to lignocellulosics, ACS Symposium Series 855. American Chemical Society, Washington DC, pp 230–243
Hildén K, Martinez AT, Hatakka A, Lundell T (2005) The two manganese peroxidases Pr-MnP2 and Pr-MnP3 of Phlebia radiata, a lignin-degrading basidiomycete, are phylogenetically and structurally divergent. Fungal Genet Biol 42:403–419
Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol 30:454–466
Hofrichter M, Ullrich R (2006) Heme-thiolate haloperoxidases: versatile biocatalysts with biotechnological and environmental significance. Appl Microbiol Biotechnol 71:276–288
Hofrichter M, Ullrich R (2010) New trends in fungal biooxidation. In: Hofrichter M (ed.) The Mycota, X, Industrial applications, 2nd edn. Springer, Berlin Heidelberg New York (in press)
Hofrichter M, Ziegenhagen D, Vares T, Friedrich M, Jager MG, Fritsche W, Hatakka A (1998) Oxidative decomposition of malonic acid as basis for the action of manganese peroxidase in the absence of hydrogen peroxide. FEBS Lett 434:362–366
Hofrichter M, Vares T, Kalsi M, Galkin S, Scheibner K, Fritsche W, Hatakka A (1999) Production of manganese peroxidase and organic acids and mineralization of 14C-labelled lignin (14C-DHP) during solid-state fermentation of wheat straw with the white rot fungus Nematoloma frowardii. Appl Environ Microbiol 65:1864–1870
Hofrichter M, Lundell T, Hatakka A (2001) Conversion of milled pine wood by manganese peroxidase from Phlebia radiata. Appl Environ Microbiol 67:4588–4593
Hofrichter M, Ullrich R, Pecyna M, Kinne M, Kluge M, Aranda E, Liers C, Poraj-Kobielska M, Gröbe G, Scheibner K, Bittner B, Piontek K, Schubert R, Hammel K (2009) Aromatic peroxygenases from mushrooms: extracellular heme-thiolate proteins of a new enzyme sub-subclass? In: Shoun H, Ohkawa H (eds), 16th International Conference on Cytochrome P450 (Nago, Okinawa, Japan), Medimond (International Proceedings), Bologna, (Italy), pp. 83–88
Horn A (2009) The use of a novel peroxidase from the basidiomycete Agrocybe aegerita as an example of enatioselective sulfoxidation (Der Einsatz einer neuartigen Peroxidase des Basidiomyceten Agrocybe aegerita am Beispiel der enatioselektiven Sulfoxidation). Dissertation, University of Rostock
Houborg K, Harris P, Poulsen JC, Schneider P, Svendsen A, Larsen S (2003) The structure of a mutant enzyme of Coprinus cinereus peroxidase provides an understanding of its increased thermostability. Acta Crystallogr D Biol Crystallogr 59:997–1003
Huang Q, Huang Q, Pinto RA, Griebenow K, Schweitzer-Stenner R, Weber WJ Jr (2005) Inactivation of horseradish peroxidase by phenoxyl radical attack. J Am Chem Soc 127:1431–1437
Huang ST, Tzean SS, Tsai BY, Hsieh HJ (2009) Cloning and heterologous expression of a novel ligninolytic peroxidase gene from poroid brown-rot fungus Antrodia cinnamomea. Microbiology 155:424–433
Husain Q, Husain M, Kulshrestha Y (2009) Remediation and treatment of organopollutants mediated by peroxidases: a review. Crit Rev Biotechnol 29:94–119
Ikehata K, Buchanan ID (2002) Screening of Coprinus species for the production of extracellular peroxidase and evaluation of the enzyme for the treatment of aqueous phenol. Environ Technol 23:1355–1367
Ishimaru A, Yamazaki I (1977) Hydroperoxide-dependent hydroxylation involving "H2O2-reducible hemoprotein" in microsomes of pea seeds. A new type enzyme acting on hydroperoxide and a physiological role of seed lipoxygenase. J Biol Chem 252:6118–6124
Johansson T, Nyman PO (1993) Isozymes of lignin peroxidase and manganese(II) peroxidase from the white-rot basidiomycete Trametes versicolor. I. Isolation of enzyme forms and characterization of physical and catalytic properties. Arch Biochem Biophys 300:49–56
Jongbloed JD, Grieger U, Antelmann H, Hecker M, Nijland R, Bron S, van Dijl JM (2004) Two minimal Tat translocases in Bacillus. Mol Microbiol 54:1319–1325
Joo H, Lin Z, Arnold FH (1999) Laboratory evolution of peroxide-mediated cytochrome P450 hydroxylation. Nature 399:670–673
Joshi DK, Gold MH (1993) Degradation of 2, 4, 5-trichlorophenol by the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 59:1779–1785
Juliána MC, Aceroa J, Salazara O, Keijerb J, Rubio V (1999) Mating type-correlated molecular markers and demonstration of heterokaryosis in the phytopathogenic fungus Thanatephorus cucumeris (Rhizoctonia solani) AG 1-IC by AFLP DNA fingerprinting analysis. J Biotech 67:49–56
Jung D, Paradiso M, Wallacher D, Brandt A, Hartmann M (2009) Formation of cross-linked chloroperoxidase aggregates in the pores of mesocellular foams: characterization by SANS and catalytic properties. ChemSusChem 2:161–164
Kauffmann C, Petersen BR, Bjerrum MJ (1999) Enzymatic removal of phenols from aqueous solutions by Coprinus cinereus peroxidase and hydrogen peroxide. J Biotechnol 73:71–74
Kaup BA, Ehrich K, Pescheck M, Schrader J (2008) Microparticle-enhanced cultivation of filamentous microorganisms: increased chloroperoxidase formation by Caldariomyces fumago as an example. Biotechnol Bioeng 99:491–498
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
Kim SJ, Shoda M (1999a) Decolorization of molasses and a dye by a newly isolated strain of the fungus Geotrichum candidum Dec 1. Biotechnol Bioeng 62:114–119
Kim SJ, Shoda M (1999b) Purification and characterization of a novel peroxidase from Geotrichum candidum Dec 1 involved in decolorization of dyes. Appl Environ Microbiol 65:1029–1035
Kim SJ, Ishikawa K, Hirai M, Shoda M (1995) Characteristics of a newly isolated fungus, Geotrichum candidum Dec 1, which decolorizes various dyes. J Ferment Bioeng 79:601–607
Kim YH, An ES, Park SY, Lee J-O, Kim JH, Song BK (2007) Polymerization of bisphenol a using Coprinus cinereus peroxidase (CiP) and its application as a photoresist resin. J Mol Cat B 44:149–154
Kim HS, Cho DH, Won K, Kim YH (2009) Inactivation of Coprinus cinereus peroxidase during the oxidation of various phenolic compounds originated from lignin. Enzyme Microb Technol 45:150–155
Kinne M, Ullrich R, Hammel KE, Hofrichter M (2008) Regioselective preparation of (R)-2-(4-Hydroxyphenoxy)propionic acid with a fungal peroxygenase. Tetrahedron Lett 49:5950–5953
Kinne M, Poraj-Kobielska M, Aranda E, Ullrich R, Hammel KE, Scheibner K, Hofrichter M (2009a) Regioselective preparation of 5-hydroxypropranolol and 4′-hydroxydiclofenac with a fungal peroxygenase. Bioorg Med Chem Lett 19:3085–3087
Kinne M, Poraj-Kobielska M, Ralph SA, Ullrich R, Hofrichter M, Hammel KE (2009b) Oxidative cleavage of diverse ethers by an extracellular fungal peroxygenase. J Biol Chem 284:29343–29349
Kinne M, Zeisig C, Ullrich R, Kayser G, Hammel KE, Hofrichter M (2010) Stepwise oxygenations of toluene and 4-nitrotoluene by a fungal peroxygenase. Biochem Byophys Res Comm (accepted)
Kjalke M, Andersen MB, Schneider P, Christensen B, Schulein M, Welinder KG (1992) Comparison of structure and activities of peroxidases from Coprinus cinereus, Coprinus macrorhizus and Arthromyces ramosus. Biochim Biophys Acta 1120:248–256
Klebanoff SJ (2005) Myeloperoxidase: friend and foe. J Leukoc Biol 77:598–625
Klibanov AM (2003) Asymmetric enzymatic oxidoreductions in organic solvents. Curr Opin Biotechnol 14:427–431
Kluge MG, Ullrich R, Scheibner K, Hofrichter M (2007) Spectrophotometric assay for detection of aromatic hydroxylation catalyzed by fungal haloperoxidase-peroxygenase. Appl Microbiol Biotechnol 75:1473–1478
Kluge M, Ullrich R, Dolge C, Scheibner K, Hofrichter M (2009) Hydroxylation of naphthalene by aromatic peroxygenase from Agrocybe aegerita proceeds via oxygen transfer from H2O2 and intermediary epoxidation. Appl Microbiol Biotechnol 81:1071–1076
Kolkman MA, van der Ploeg R, Bertels M, van Dijk M, van der Laan J, van Dijl JM, Ferrari E (2008) The twin-arginine signal peptide of Bacillus subtilis YwbN can direct either Tat- or Sec-dependent secretion of different cargo proteins: secretion of active subtilisin via the B. subtilis Tat pathway. Appl Environ Microbiol 74:7507–7513
Koskiniemi H, Metsa-Ketela M, Dobritzsch D, Kallio P, Korhonen H, Mantsala P, Schneider G, Niemi J (2007) Crystal structures of two aromatic hydroxylases involved in the early tailoring steps of angucycline biosynthesis. J Mol Biol 372:633–648
Kuan IC, Tien M (1993) Stimulation of Mn peroxidase activity: a possible role for oxalate in lignin biodegradation. Proc Natl Acad Sci U S A 90:1242–1246
Kühnel K, Blankenfeldt W, Terner J, Schlichting I (2006) Crystal structures of chloroperoxidase with its bound substrates and complexed with formate, acetate, and nitrate. J Biol Chem 281:23990–23998
Kunishima N, Fukuyama K, Matsubara H, Hatanaka H, Shibano Y, Amachi T (1994) Crystal structure of the fungal peroxidase from Arthromyces ramosus at 1.9 A resolution. Structural comparisons with the lignin and cytochrome c peroxidases. J Mol Biol 235:331–344
Lambeir AM, Dunford HB (1983) A kinetic and spectral study of the alkaline transitions of chloroperoxidase. Arch Biochem Biophys 220:549–556
Lankinen P, Hildén K, Aro N, Salkinoja-Salonen M, Hatakka A (2005) Manganese peroxidase of Agaricus bisporus: grain bran-promoted production and gene characterization. Appl Microbiol Biotechnol 66:401–407
Larrondo L, Gonzalez A, Perez Acle T, Cullen D, Vicuna R (2005) The nop gene from Phanerochaete chrysosporium encodes a peroxidase with novel structural features. Biophys Chem 116:167–173
Leak DJ, Sheldon RA, Woodley JM, Adlercreutz P (2009) Biocatalysts for selective introduction of oxygen. Biocat Biotrans 27:1–26
Libby RD, Thomas JA, Kaiser LW, Hager LP (1982) Chloroperoxidase halogenation reactions. Chemical versus enzymic halogenating intermediates. J Biol Chem 257:5030–5037
Liers C, Ullrich R, Kinne M, Pecyna M, Kluge M, Aranda E, Scheibner K, Hofrichter M (2009) Oxidation of non-phenolic lignin model compounds by novel fungal peroxidases. Proceedings book of the INTB Conference on "Biotechnological Functionalisation of Advanced Fibre Reinforced Composites". University of Ghent, Ghent, pp. 238–243
Liers C, Bobeth C, Pecyna M, Ullrich R, Hofrichter M (2010) DyP-like peroxidases of the jelly fungus Auricularia auricula-judae oxidize nonphenolic lignin model compounds and high-redox potential dyes. Appl Microbiol Biotechnol 85:1869–1879
Littlechild J (1999) Haloperoxidases and their role in biotransformation reactions. Curr Opin Chem Biol 3:28–34
Liu JZ, Wang M (2007) Improvement of activity and stability of chloroperoxidase by chemical modification. BMC Biotechnol 7:23
Liu KK-C, Wong C-H (1992) Enzymatic halohydration of glycals. J Org Chem 57:3748–3750
Longoria A, Tinoco R, Vázquez-Duhalt R (2008) Chloroperoxidase-mediated transformation of highly halogenated monoaromatic compounds. Chemosphere 72:485–490
Longoria AM, Hu H, Vazquez-Duhalt R (2009) Enzymatic synthesis of semiconductor polymers by chloroperoxidase of Caldariomyces fumago. Appl Biochem Biotechnol. doi:10.1007/s12010-009-8805-7
Lundell T (1993) Ligninolytic system of the white-rot fungus Phlebia radiata: Lignin model compound studies. Ph.D. Thesis (dissertation), Department of Applied Chemistry and Microbiology, University of Helsinki (Finland)
Lundell T, Schoemaker H, Hatakka A, Brunow G (1993a) New mechanism of the Cα-Cβ cleavage in non-phenolic arylglycerol β-aryl ether lignin substructures catalyzed by lignin peroxidase. Holzforschung 47:219–224
Lundell T, Wever R, Floris R, Harvey P, Hatakka A, Brunow G, Schoemaker H (1993b) Lignin peroxidase L3 from Phlebia radiata. Pre-steady-state and steady-state studies with veratryl alcohol and a non-phenolic lignin model compound 1-(3, 4-dimethoxyphenyl)-2-(2-methoxyphenoxy)propane-1, 3-diol. Eur J Biochem 211:391–402
Lundell TK, Mäkelä MR, Hildén K (2010) Lignin-modifying enzymes in filamentous basidiomycetes: ecological, functional and phylogenetic review. J Basic Microbiol 50:1–16
Makris TM, Denisov I, Schlichting I, Sligar SG (2005) Activation of molecular oxygen by cytochrome P450. In: Ortiz De Montellano PR (ed) Cytochrome P450 - structure, mechanism and biochemistry, 3rd edn. Kluwer Academic/Plenum Publishers, New York, pp 149–182
Manoj KM (2006) Chlorinations catalyzed by chloroperoxidase occur via diffusible intermediate(s) and the reaction components play multiple roles in the overall process. Biochim Biophys Acta 1764:1325–1339
Manoj KM, Hager LP (2006) A colorimetric method for detection and quantification of chlorinating activity of hemeperoxidases. Anal Biochem 348:84–86
Manoj KM, Hager LP (2008) Chloroperoxidase, a janus enzyme. Biochemistry 47:2997–3003
Manoj KM, Lakner FJ, Hager LP (2000) Epoxidation of indene by chloroperoxidase. J Mol Catal B Enzym 9:107–111
Marjamaa K, Hildén K, Kukkola E, Lehtonen M, Holkeri H, Haapaniemi P, Koutaniemi S, Teeri TH, Fagerstedt K, Lundell T (2006) Cloning, characterization and localization of three novel class III peroxidases in lignifying xylem of Norway spruce (Picea abies). Plant Mol Biol 61:719–732
Martin F, Aerts A, Ahrén D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbé J, Lin YC, Legué V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouzé P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92
Martínez AT (2002) Molecular biology and structure-function of lignin-degrading heme peroxidases. Enzyme Microb Technol 30:425–444
Martínez AT (2007) High redox potential peroxidases. In: Polaina J, MacCabe AP (eds) Industrial enzymes: structure, function and applications, 1st edn. Springer-Verlag, Berlin, pp 475–486
Martínez AT, Speranza M, Ruiz-Dueñas FJ, Ferreira P, Camarero S, Guillen F, Martínez MJ, Gutiérrez A, del Río JC (2005) Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8:195–204
Martínez AT, Ruiz-Dueñas FJ, Martínez MJ, Del Rio JC, Gutierrez A (2009) Enzymatic delignification of plant cell wall: from nature to mill. Curr Opin Biotechnol 20:348–357
Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22:695–700
Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Vanden Wymelenberg A, Gaskell J, Lindquist E, Sabat G, Bondurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavín JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kües U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci U S A 106:1954–1959
Martínez MJ, Böckle B, Camarero S, Guillén F, Martínez AT (1996) MnP isoenzymes produced by two Pleurotus species in liquid culture and during wheat-straw solid-state fermentation ACS Symposium Series 655. American Chemical Society, Washington DC, pp 183–196
Mester T, Field JA (1998) Characterization of a novel manganese peroxidase-lignin peroxidase hybrid isozyme produced by Bjerkandera species strain BOS55 in the absence of manganese. J Biol Chem 273:15412–15417
Michels J, Gottschalk G (1994) Inhibition of the lignin peroxidase of Phanerochaete chrysosporium by hydroxylamino-dinitrotoluene, an early intermediate in the degradation of 2, 4, 6-trinitrotoluene. Appl Environ Microbiol 60:187–194
Miki K, Renganathan V, Gold MH (1986) Mechanism of β-aryl ether dimeric lignin model compound oxidation by lignin peroxidase of Phanerochaete chrysosporium. Biochemistry 25:4790–4796
Miki K, Renganathan V, Mayfield MB, Gold MH (1987) Aromatic ring cleavage of a β-biphenyl ether dimer catalyzed by lignin peroxidase of Phanerochaete chrysosporium. FEBS Lett 210:199–203
Miki Y, Tanaka H, Nakamura M, Wariishi Y (2006) Isolation and characterization of a novel lignin peroxidase from the white-rot basidiomycete Trametes cervina. J Fac Agr Kyushy Univ 51:99–104
Miki Y, Morales M, Ruiz-Dueñas FJ, Martínez MJ, Wariishi H, Martínez AT (2009) Escherichia coli expression and in vitro activation of a unique ligninolytic peroxidase that has a catalytic tyrosine residue. Protein Expr Purif 68:208–214
Moilanen A-M, Lundell T, Vares T, Hatakka A (1996) Manganese and malonate are individual regulators for the production of lignin and manganese peroxidase isozymes and in the degradation of lignin by Phlebia radiata. Appl Microbiol Biotechnol 45:792–799
Moreira PR, Duez C, Dehareng D, Antunes A, Almeida-Vara E, Frère JM, Malcata FX, Duarte JC (2005) Molecular characterisation of a versatile peroxidase from a Bjerkandera strain. J Biotechnol 118:339–352
Morgan JA, Lu Z, Clark DS (2002) Toward the development of a biocatalytic system for oxidation of p-xylene to terephthalic acid: oxidation of 1, 4-benzenedimethanol. J Mol Catal B: Enz 18:147–154
Morgenstern I, Klopman S, Hibbett DS (2008) Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes. J Mol Evol 66:243–257
Morris DR, Hager LP (1966) Chloroperoxidase. I. Isolation and properties of the crystalline glycoprotein. J Biol Chem 241:1763–1768
Neidleman SL, Diassi PA, Junta B, Palmere RM, Pan SC (1966) The enzymatic halogenation of steroids. Tetrahedron Lett 44:5337–5342
Newcomb M, Aebisher D, Shen R, Chandrasena RE, Hollenberg PF, Coon MJ (2003) Kinetic isotope effects implicate two electrophilic oxidants in cytochrome p450-catalyzed hydroxylations. J Am Chem Soc 125:6064–6065
Nonaka D, Wariishi H, Welinder KG, Fujii H (2010) Paramagnetic 13C and 15N NMR analyses of the push and pull effects in cytochrome c peroxidase and Coprinus cinereus peroxidase variants: functional roles of highly conserved amino acids around heme. Biochemistry 49:49–57
Nuell MJ, Fang GH, Axley MJ, Kenigsberg P, Hager LP (1988) Isolation and nucleotide sequence of the chloroperoxidase gene from Caldariomyces fumago. J Bacteriol 170:1007–1011
Ogola HJ, Kamiike T, Hashimoto N, Ashida H, Ishikawa T, Shibata H, Sawa Y (2009) Molecular characterization of a novel peroxidase from the cyanobacterium Anabaena sp. strain PCC 7120. Appl Environ Microbiol 75:7509–7518
Oliva M, Theiler G, Zamocky M, Koua D, Margis-Pinheiro M, Passardi F, Dunand C (2009) PeroxiBase: a powerful tool to collect and analyse peroxidase sequences from Viridiplantae. J Exp Bot 60:453–459
Omura T (2005) Heme-thiolate proteins. Biochem Biophys Res Commun 338:404–409
Omura T (2010) Structural diversity of cytochrome P450 enzyme systems. J Biotechnol 147:297–306
Ortiz de Montellano P (2005) Cytochrome P450 - structure, mechanism and biochemistry, 3rd edn. Kluwer Academic/Plenum Publishers, New York
Ortiz de Montellano PR, de Voss JJ (2005) Substrate oxidation by cytochrome P450 enzymes. In: Ortiz De Montellano PR (ed) Cytochrome P450 - structure, mechanism and biochemistry, 3rd edn. Kluwer Academic/Plenum Publishers, New York, pp 183–245
Ortiz-Bermudez P, Srebotnik E, Hammel KE (2003) Chlorination and cleavage of lignin structures by fungal chloroperoxidases. Appl Environ Microbiol 69:5015–5018
Ortiz-Bermudez P, Hirth KC, Srebotnik E, Hammel KE (2007) Chlorination of lignin by ubiquitous fungi has a likely role in global organochlorine production. Proc Natl Acad Sci U S A 104:3895–3900
Osborne RL, Coggins MK, Terner J, Dawson JH (2007) Caldariomyces fumago chloroperoxidase catalyzes the oxidative dehalogenation of chlorophenols by a mechanism involving two one-electron steps. J Am Chem Soc 129:14838–14389
Otey CR, Landwehr M, Endelman JB, Hiraga K, Bloom JD, Arnold FH (2006) Structure-guided recombination creates an artificial family of cytochromes P450. PLoS Biol 4:e112
Park JB, Clark DS (2006) Deactivation mechanisms of chloroperoxidase during biotransformations. Biotechnol Bioeng 93:1190–1195
Partridge M, Murphy DJ (2009) Roles of a membrane-bound caleosin and putative peroxygenase in biotic and abiotic stress responses in Arabidopsis. Plant Physiol Biochem 47:796–806
Passardi F, Bakalovic N, Teixeira FK, Margis-Pinheiro M, Penel C, Dunand C (2007a) Prokaryotic origins of the non-animal peroxidase superfamily and organelle-mediated transmission to eukaryotes. Genomics 89:567–579
Passardi F, Theiler G, Zamocky M, Cosio C, Rouhier N, Teixera F, Margis-Pinheiro M, Ioannidis V, Penel C, Falquet L, Dunand C (2007b) PeroxiBase: the peroxidase database. Phytochemistry 68:1605–1611
Pecyna MJ, Schnorr KM, Ullrich R, Scheibner K, Kluge M, Hofrichter M (2008) Fungal peroxygenases and methods of application. patent, WO 2008/119780 A2
Pecyna MJ, Ullrich R, Bittner B, Clemens A, Scheibner K, Schubert R, Hofrichter M (2009) Molecular characterization of aromatic peroxygenase from Agrocybe aegerita. Appl Microbiol Biotechnol 84:885–897
Peng L, Wollenberger U, Hofrichter M, Ullrich R, Scheibner K, Scheller FW (2009) Bioelectrocatalytic properties of Agrocybe aegerita peroxygenase. Electrochimica Acta. doi:10.1016/j.electacta.2009.12.065
Perez DI, Grau MM, Arends IW, Hollmann F (2009) Visible light-driven and chloroperoxidase-catalyzed oxygenation reactions. Chem Commun (Camb):6848-6850
Pérez-Boada M, Ruiz-Dueñas FJ, Pogni R, Basosi R, Choinowski T, Martínez MJ, Piontek K, Martínez AT (2005) Versatile peroxidase oxidation of high redox potential aromatic compounds: site-directed mutagenesis, spectroscopic and crystallographic investigation of three long-range electron transfer pathways. J Mol Biol 354:385–402
Petersen JF, Kadziola A, Larsen S (1994) Three-dimensional structure of a recombinant peroxidase from Coprinus cinereus at 2.6 A resolution. FEBS Lett 339:291–296
Petrides PE, Nauseef WM (2000) The peroxidase multigene family of enzymes: Biochemical basis and clinical applications 1st edn. Springer-Verlag, Berlin Heidelberg
Piontek K, Glumoff T, Winterhalter K (1993) Low pH crystal structure of glycosylated lignin peroxidase from Phanerochaete chrysosporium at 2.5 A resolution. FEBS Lett 315:119–124
Piontek K, Smith AT, Blodig W (2001) Lignin peroxidase structure and function. Biochem Soc Trans 29:111–116
Piontek K, Ullrich R, Liers C, Diederichs K, Plattner D, Hofrichter M (2010) Crystallization of a 45 kDa peroxygenase/peroxidase from the mushroom Agrocybe aegerita and structure determination by SAD utilizing only the haem iron. Acta Crystallogr Sect F Struct Biol Cryst Commun 66: doi:10.1107/S1744309110013515
Poulos TL (1993) Peroxidases. Curr Opin Biotechnol 4:484–489
Poulos TL, Freer ST, Alden RA, Xuong NH, Edwards SL, Hamlin RC, Kraut J (1978) Crystallographic determination of the heme orientation and location of the cyanide binding site in yeast cytochrome c peroxidase. J Biol Chem 253:3730–3735
Poulos TL, Edwards SL, Wariishi H, Gold MH (1993) Crystallographic refinement of lignin peroxidase at 2 A. J Biol Chem 268:4429–4440
Prieto MA, Perez-Aranda A, Garcia JL (1993) Characterization of an Escherichia coli aromatic hydroxylase with a broad substrate range. J Bacteriol 175:2162–2167
Pühse M, Szweda RT, Ma Y, Jeworrek C, Winter R, Zorn H (2009) Marasmius scorodonius extracellular dimeric peroxidase—exploring its temperature and pressure stability. Biochim Biophys Acta 1794:1091–1098
Que L Jr, Tolman WB (2008) Biologically inspired oxidation catalysis. Nature 455:333–340
Ramakrishnan K, Oppenhuizen ME, Saunders S, Fisher J (1983) Stereoselectivity of chloroperoxidase-dependent halogenation. Biochemistry 22:3271–3277
Reynolds DR, Faull JL (2001) Proposals to conserve the name Caldariomyces against Leptoxyphium and the name C. fumago with a conserved type (Ascomycota, mitosporic Euascomycetes). Taxon 50:1183–1184
Robertson DE, Richardson T, Kustedjo K, Amitai G, Lejeune K, Berberich J, Chaplin JA, Sinclair J (2008) Enzymes and formulations for broad-specificity decontamination of chemical and biological warfare agents. patent, WO/2008/036061
Ruiz-Dueñas FJ, Martínez MJ, Martínez AT (1999) Molecular characterization of a novel peroxidase isolated from the ligninolytic fungus Pleurotus eryngii. Mol Microbiol 31:223–235
Ruiz-Dueñas FJ, Morales M, Mate MJ, Romero A, Martínez MJ, Smith AT, Martínez AT (2008) Site-directed mutagenesis of the catalytic tryptophan environment in Pleurotus eryngii versatile peroxidase. Biochemistry 47:1685–1695
Ruiz-Dueñas FJ, Morales M, Garcia E, Miki Y, Martínez MJ, Martínez AT (2009) Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J Exp Bot 60:441–452
Sakurai T, Kataoka K (2007) Basic and applied features of multicopper oxidases, CueO, bilirubin oxidase, and laccase. Chem Rec 7:220–229
Sanfilippo C, Nicolosi G (2002) Catalytic behaviour of chloroperoxidase from Caldariomyces fumago in the oxidation of cyclic conjugated dienes. Tetrahedron Asymmetr 13:1889–1892
Sanfilippo C, D'Antona N, Nicolosi G (2004) Chloroperoxidase from Caldariomyces fumago is active in the presence of an ionic liquid as co-solvent. Biotechnol Lett 26:1815–1819
Sasaki S, Nonaka D, Wariishi H, Tsutsumi Y, Kondo R (2008) Role of Tyr residues on the protein surface of cationic cell-wall-peroxidase (CWPO-C) from poplar: potential oxidation sites for oxidative polymerization of lignin. Phytochemistry 69:348–355
Sato T, Hara S, Matsui T, Sazaki G, Saijo S, Ganbe T, Tanaka N, Sugano Y, Shoda M (2004) A unique dye-decolorizing peroxidase, DyP, from Thanatephorus cucumeris Dec 1: heterologous expression, crystallization and preliminary X-ray analysis. Acta Crystallogr D Biol Crystallogr 60:149–152
Savitsky PA, Gazaryan IG, Tishkov VI, Lagrimini LM, Ruzgas T, Gorton L (1999) Oxidation of indole-3-acetic acid by dioxygen catalysed by plant peroxidases: specificity for the enzyme structure. Biochem J 340(Pt3):579–583
Scheibner M, Hulsdau B, Zelena K, Nimtz M, de Boer L, Berger RG, Zorn H (2008) Novel peroxidases of Marasmius scorodonius degrade beta-carotene. Appl Microbiol Biotechnol 77:1241–1250
Schmid RD, Urlacher V (2007) Modern biooxidation enzymes, reactions and applications, 1st edn. Wiley-VCH, Weinheim
Schoemaker HE, Lundell T, Hatakka A, Piontek K (1994) The oxidation of veratryl alcohol, dimeric lignin models and lignin by lignin peroxidase: the redox cycle revisioned. FEMS Microbiol Rev 13:321–332
Schomburg D, Schomburg I (2006) Class 1 oxidoreductases X. Springer handbook of enzymes, 2nd edn., vol. 25. Springer-Verlag, Berlin, Heidelberg
Seelbach K, van Deurzen MP, van Rantwijk F, Sheldon RA, Kragl U (1997) Improvement of the total turnover number and space-time yield for chloroperoxidase catalyzed oxidation. Biotechnol Bioeng 55:283–288
Shaw PD, Hager LP (1959) Biological chlorination. III. beta-Ketoadipate chlorinase: a soluble enzyme system. J Biol Chem 234:2565–2569
Shimokawa T, Shoda M, Sugano Y (2009) Purification and characterization of two DyP isozymes from Thanatephorus cucumeris Dec 1 specifically expressed in an air-membrane surface bioreactor. J Biosci Bioeng 107:113–115
Singer R (1949) The Agaricales in modern taxonomy. Lilloa 22:1–832, published in 1951
Smith AT, Doyle WA (2006) Engineered peroxidases with veratryl alcohol oxidase activity. patent, WO/2006/114616
Smith AT, Doyle WA, Dorlet P, Ivancich A (2009) Spectroscopic evidence for an engineered, catalytically active Trp radical that creates the unique reactivity of lignin peroxidase. Proc Natl Acad Sci U S A 106:16084–16089
Sturm A, Schierhorn A, Lindenstrauss U, Lilie H, Bruser T (2006) YcdB from Escherichia coli reveals a novel class of Tat-dependently translocated hemoproteins. J Biol Chem 281:13972–13978
Sugano Y (2009) DyP-type peroxidases comprise a novel heme peroxidase family. Cell Mol Life Sci 66:1387–1403
Sugano Y, Sasaki K, Shoda M (1999) cDNA cloning and genetic analysis of a novel decolorizing enzyme, peroxidase gene dyp from Geotrichum candidum Dec 1. J Biosci Bioeng 87:411–417
Sugano Y, Nakano R, Sasaki K, Shoda M (2000) Efficient heterologous expression in Aspergillus oryzae of a unique dye-decolorizing peroxidase, DyP, of Geotrichum candidum Dec 1. Appl Environ Microbiol 66:1754–1758
Sugano Y, Muramatsu R, Ichiyanagi A, Sato T, Shoda M (2007) DyP, a unique dye-decolorizing peroxidase, represents a novel heme peroxidase family: ASP171 replaces the distal histidine of classical peroxidases. J Biol Chem 282:36652–36658
Sugano Y, Matsushima Y, Tsuchiya K, Aoki H, Hirai M, Shoda M (2009) Degradation pathway of an anthraquinone dye catalyzed by a unique peroxidase DyP from Thanatephorus cucumeris Dec 1. Biodegradation 20:433–440
Sugiura T, Yamagishi K, Kimura T, Nishida T, Kawagishi H, Hirai H (2009) Cloning and homologous expression of novel lignin peroxidase genes in the white-rot fungus Phanerochaete sordida YK-624. Biosci Biotechnol Biochem 73:1793–1798
Sundaramoorthy M, Kishi K, Gold MH, Poulos TL (1994) The crystal structure of manganese peroxidase from Phanerochaete chrysosporium at 2.06-A resolution. J Biol Chem 269:32759–32767
Sundaramoorthy M, Terner J, Poulos TL (1995) The crystal structure of chloroperoxidase: a heme peroxidase–cytochrome P450 functional hybrid. Structure 3:1367–1377
Sundaramoorthy M, Youngs HL, Gold MH, Poulos TL (2005) High-resolution crystal structure of manganese peroxidase: substrate and inhibitor complexes. Biochemistry 44:6463–6470
Suske WA, Held M, Schmid A, Fleischmann T, Wubbolts MG, Kohler HP (1997) Purification and characterization of 2-hydroxybiphenyl 3-monooxygenase, a novel NADH-dependent, FAD-containing aromatic hydroxylase from Pseudomonas azelaica HBP1. J Biol Chem 272:24257–24265
Syoda M, Sugano Y, Kubota H (2006) Enzyme having decolorizing activity and method for decolorizing dyes by using the same. patent, 7041486 B1
Tassaneeyakul W, Veronese ME, Birkett DJ, Gonzalez FJ, Miners JO (1993) Validation of 4-nitrophenol as an in vitro substrate probe for human liver CYP2E1 using cDNA expression and microsomal kinetic techniques. Biochem Pharmacol 46:1975–1981
ten Have R, Hartmans S, Teunissen PJ, Field JA (1998) Purification and characterization of two lignin peroxidase isozymes produced by Bjerkandera sp. strain BOS55. FEBS Lett 422:391–394
Tien M, Kirk TK (1988) Lignin peroxidase of Phanerochaete chrysosporium. Meth Enzymol 161:238–249
Tien M, Kirk TK, Bull C, Fee JA (1986) Steady-state and transient-state kinetic studies on the oxidation of 3, 4-dimethoxybenzyl alcohol catalyzed by the ligninase of Phanerocheate chrysosporium Burds. J Biol Chem 261:1687–1693
Torres Pazmiño DE, Dudek HM, Fraaije MW (2009) Baeyer–Villiger monooxygenases: recent advances and future challenges. Curr Opin Chem Biol 14:1–7
Tuisel H, Sinclair R, Bumpus JA, Ashbaugh W, Brock BJ, Aust SD (1990) Lignin peroxidase H2 from Phanerochaete chrysosporium: purification, characterization and stability to temperature and pH. Arch Biochem Biophys 279:158–166
Ullrich R, Hofrichter M (2005) The haloperoxidase of the agaric fungus Agrocybe aegerita hydroxylates toluene and naphthalene. FEBS Lett 579:6247–6250
Ullrich R, Hofrichter M (2007) Enzymatic hydroxylation of aromatic compounds. Cell Mol Life Sci 64:271–293
Ullrich R, Nüske J, Scheibner K, Spantzel J, Hofrichter M (2004) Novel haloperoxidase from the agaric basidiomycete Agrocybe aegerita oxidizes aryl alcohols and aldehydes. Appl Environ Microbiol 70:4575–4581
Ullrich R, Dolge C, Kluge M, Hofrichter M (2008) Pyridine as novel substrate for regioselective oxygenation with aromatic peroxygenase from Agrocybe aegerita. FEBS Lett 582:4100–4106
Ullrich R, Liers C, Schimpke S, Hofrichter M (2009) Purification of homogeneous forms of fungal peroxygenase. Biotechnol J 4:1619–1626
Urzúa U, Kersten PJ, Vicuña R (1998) Manganese peroxidase-dependent oxidation of glyoxylic and oxalic acids synthesized by Ceriporiopsis subvermispora produces extracellular hydrogen peroxide. Appl Environ Microbiol 64:68–73
van Bloois E, Torres Pazmiño DE, Winter RT, Fraaije MW (2009) A robust and extracellular heme-containing peroxidase from Thermobifida fusca as prototype of a bacterial peroxidase superfamily. Appl Microbiol Biotechnol. doi:10.1007/s00253-009-2369-x
van de Velde F, Bakker M, van Rantwijk F, Sheldon RA (2001) Chloroperoxidase-catalyzed enantioselective oxidations in hydrophobic organic media. Biotechnol Bioeng 72:523–529
van der Veen BS, de Winther MP, Heeringa P (2009) Myeloperoxidase: molecular mechanisms of action and their relevance to human health and disease. Antioxid Redox Signal 11:2899–2937
van Peé KH (2001) Microbial biosynthesis of halometabolites. Arch Microbiol 175:250–258
van Peé KH, Zehner S (2003) Enzymology and molecular genetics of biological halogenation. In: Gribble GW (ed) Natural production of organohalogen compounds, 1st edn. Springer-Verlag, Berlin, Heidelberg, pp 171–199
van Rantwijk F, Sheldon RA (2000) Selective oxygen transfer catalysed by heme peroxidases: synthetic and mechanistic aspects. Curr Opin Biotechnol 11:554–564
Vares T, Niemenmaa O, Hatakka A (1994) Secretion of ligninolytic enzymes and mineralization of 14C-ring-labelled synthetic lignin by three Phlebia tremellosa strains. Appl Environ Microbiol 60:569–575
Vázquez-Duhalt R, del Pilar Bremauntz M, Barzana E, Tinoco R (2002) Enzymatic oxidation process for desulfurization of fossil fuels. patent, 6461859 B1
Wagner C, Molitor IM, Konig GM (2008) Critical view on the monochlorodimedone assay utilized to detect haloperoxidase activity. Phytochemistry 69:323–332
Wang W, Xu Y, Wang DI, Li Z (2009) Recyclable nanobiocatalyst for enantioselective sulfoxidation: facile fabrication and high performance of chloroperoxidase-coated magnetic nanoparticles with iron oxide core and polymer shell. J Am Chem Soc 131:12892–12893
Wariishi H, Gold MH (1990) Lignin peroxidase compound III. Mechanism of formation and decomposition. J Biol Chem 265:2070–2077
Wariishi H, Valli K, Gold MH (1991) In vitro depolymerization of lignin by manganese peroxidase of Phanerochaete chrysosporium. Biochem Biophys Res Commun 176:269–275
Wariishi H, Valli K, Gold MH (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. Kinetic mechanism and role of chelators. J Biol Chem 267:23688–23695
Wariishi H, Sheng D, Gold MH (1994) Oxidation of ferrocytochrome c by lignin peroxidase. Biochemistry 33:5545–5552
Welinder K (1992) Plant peroxidases: structure–function relationships. In: Penel C, Gaspar T, Greppin H (eds) Plant peroxidases, topics and detailed literature on molecular, biochemical and physiological aspects. Université de Genève, Genève, pp 1–24
Wesenberg D, Kyriakides I, Agathos SN (2003) White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Adv 22:161–187
Wilson AW, Desjardin DE (2005) Phylogenetic relationships in the gymnopoid and marasmioid fungi (Basidiomycetes, euagarics clade). Mycologia 97:667–679
Xu F (2005) Applications of oxidoreductases: recent progress. Ind Biotechnol 1:38–50
Young L, Yu J (1997) Ligninase-catalysed decolorization of synthetic dyes. Water Res 31:1187–1193
Zamocky M, Jakopitsch C, Furtmuller PG, Dunand C, Obinger C (2008) The peroxidase-cyclooxygenase superfamily: Reconstructed evolution of critical enzymes of the innate immune system. Proteins 72:589–605
Zamocky M, Furtmuller PG, Obinger C (2009) Two distinct groups of fungal catalase/peroxidases. Biochem Soc Trans 37:772–777
Zelena K, Hardebusch B, Hulsdau B, Berger RG, Zorn H (2009a) Generation of norisoprenoid flavors from carotenoids by fungal peroxidases. J Agric Food Chem 57:9951–9955
Zelena K, Zorn H, Nimtz M, Berger RG (2009b) Heterologous expression of the msp2 gene from Marasmius scorodonius. Arch Microbiol 191:397–402
Zhang LH, Bai CH, Wang YS, Jiang YC, Hu MC, Li SN, Zhai QG (2009) Improvement of chloroperoxidase stability by covalent immobilization on chitosan membranes. Biotechnol Lett 31:1269–1272
Zorn H, Scheibner M, Hülsdau B, Berger RG, de Boer L, Meima RB (2005) Novel enzymes for use in enzymatic bleaching of food products. patent, EP 64132 20060712
Zorn H, Szweda RT, Wilms J, Kumar M (2008) Method for modifying non-starch carbohydrate material. patent, 26485/EP/P0
Zubieta C, Joseph R, Krishna SS, McMullan D, Kapoor M, Axelrod HL, Miller MD, Abdubek P, Acosta C, Astakhova T, Carlton D, Chiu HJ, Clayton T, Deller MC, Duan L, Elias Y, Elsliger MA, Feuerhelm J, Grzechnik SK, Hale J, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Kumar A, Marciano D, Morse AT, Murphy KD, Nigoghossian E, Okach L, Oommachen S, Reyes R, Rife CL, Schimmel P, Trout CV, van den Bedem H, Weekes D, White A, Xu Q, Hodgson KO, Wooley J, Deacon AM, Godzik A, Lesley SA, Wilson IA (2007a) Identification and structural characterization of heme binding in a novel dye-decolorizing peroxidase, TyrA. Proteins 69:234–243
Zubieta C, Krishna SS, Kapoor M, Kozbial P, McMullan D, Axelrod HL, Miller MD, Abdubek P, Ambing E, Astakhova T, Carlton D, Chiu HJ, Clayton T, Deller MC, Duan L, Elsliger MA, Feuerhelm J, Grzechnik SK, Hale J, Hampton E, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kumar A, Marciano D, Morse AT, Nigoghossian E, Okach L, Oommachen S, Reyes R, Rife CL, Schimmel P, van den Bedem H, Weekes D, White A, Xu Q, Hodgson KO, Wooley J, Deacon AM, Godzik A, Lesley SA, Wilson IA (2007b) Crystal structures of two novel dye-decolorizing peroxidases reveal a beta-barrel fold with a conserved heme-binding motif. Proteins 69:223–233
Acknowledgments
We would like to thank our coworkers I. Kluge, M. Kinne, M. Poraj-Kobielska, S. Peter, C. Dolge, M. Rotter, and K. Barková for their support with data and their know-how. Scientific work has been supported by the European Union (integrated project Biorenew), the Deutsche Bundestiftung Umwelt (DBU, projects “Pilzliche Sekretome” and “Neuartige Peroxygenasen”), as well as the Deutsche Forschungsgemeinschaft (DFG; projects Fupers and Funwood within the Priority Programme 1374 - Biodiversity Exploratories).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hofrichter, M., Ullrich, R., Pecyna, M.J. et al. New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol 87, 871–897 (2010). https://doi.org/10.1007/s00253-010-2633-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-010-2633-0