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The ligninolytic peroxidases in the genus Pleurotus: divergence in activities, expression, and potential applications

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Abstract

Mushrooms of the genus Pleurotus are comprised of cultivated edible ligninolytic fungi with medicinal properties and a wide array of biotechnological and environmental applications. Like other white-rot fungi (WRF), they are able to grow on a variety of lignocellulosic biomass substrates and degrade both natural and anthropogenic aromatic compounds. This is due to the presence of the non-specific oxidative enzymatic systems, which are mainly consisted of lacasses, versatile peroxidases (VPs), and short manganese peroxidases (short-MnPs). Additional, less studied, peroxidase are dye-decolorizing peroxidases (DyPs) and heme-thiolate peroxidases (HTPs). During the past two decades, substantial information has accumulated concerning the biochemistry, structure and function of the Pleurotus ligninolytic peroxidases, which are considered to play a key role in many biodegradation processes. The production of these enzymes is dependent on growth media composition, pH, and temperature as well as the growth phase of the fungus. Mn2+ concentration differentially affects the expression of the different genes. It also severs as a preferred substrate for these preoxidases. Recently, sequencing of the Pleurotus ostreatus genome was completed, and a comprehensive picture of the ligninolytic peroxidase gene family, consisting of three VPs and six short-MnPs, has been established. Similar enzymes were also discovered and studied in other Pleurotus species. In addition, progress has been made in the development of molecular tools for targeted gene replacement, RNAi-based gene silencing and overexpression of genes of interest. These advances increase the fundamental understanding of the ligninolytic system and provide the opportunity for harnessing the unique attributes of these WRF for applied purposes.

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References

  • Amore A, Honda Y, Faraco V (2012) Enhanced green fluorescent protein expression in Pleurotus ostreatus for in vivo analysis of fungal laccase promoter. Appl Biochem Biotechnol 168:761–769

    CAS  PubMed  Google Scholar 

  • Arunkumara M, Sheik Abdullaa SH (2014) Hyper-production of manganese peroxidase by mutant Pleurotus ostreatus MTCC 142 and its applications in biodegradation of textile azo dyes. Desalin Water Treat. doi:10.1080/19443994.2014.937766

    Google Scholar 

  • Asada Y, Watanabe A, Irie T, Nakayama T, Kuwahara M (1995) Structures of genomic and complementary DNAs coding for Pleurotus ostreatus manganese (II) peroxidase. Biochim Biophys Acta 1251:205–209

    PubMed  Google Scholar 

  • Asgher M, Aslam B, Iqbal HMN (2013) Novel catalytic and effluent decolorization functionalities of sol–gel immobilized Pleurotus ostreatus IBL-02 manganese peroxidase produced from bio-processing of wheat straw. Chin J Catal 34:1756–1761

    CAS  Google Scholar 

  • Avin FA, Bhassu S, Tan YS, Shahbazi P, Vikineswary S (2014) Molecular divergence and species delimitation of the cultivated oyster mushroom: integration of IGS1 and ITS. Sci World J. doi:10.1155/2014/793414

    Google Scholar 

  • Bazanella GCD, de Souza DF, Castoldi R, Oliveira RF, Bracht A, Peralta RM (2013) Production of laccase and manganese peroxidase by Pleurotus pulmonarius in solid-state cultures and application in dye decolorization. Folia Microbiol 58:641–647

    CAS  Google Scholar 

  • Bezalel L, Hadar Y, Cerniglia CE (1997) Enzymatic mechanisms involved in phenanthrene degradation by the white fungus Pleurotus ostreatus. Appl Environ Microbiol 63:2495–2501

    CAS  PubMed Central  PubMed  Google Scholar 

  • Blanchette RA (1984) Screening wood decayed by white rot fungi for preferential lignin degradation. Appl Environ Microbiol 48(3):647–653

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Camarero S, Böckle B, Martínez MJ, Martínez AT (1996) Manganese-mediated lignin degradation by Pleurotus pulmonarius. Appl Environ Microbiol 62:1070–1072

    CAS  PubMed Central  PubMed  Google Scholar 

  • Camarero S, Sarkar S, Ruiz-Dueñas FJ, Martínez MJ, Martínez AT (1999) Description of a versatile peroxidase in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites. J Biol Chem 274:10324–10330

    CAS  PubMed  Google Scholar 

  • Capdevila C, Moukha S, Ghyczy M, Theilleus J, Gelie B, Delattre M, Corrieu G, Asther M (1990) Characterization of peroxidase secretion and subcellular organization of Phanerochaete chrysosporium INA-12 in the presence of various soybean phospholipid fractions. Appl Environ Microbiol 56:3811–3816

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carabajal M, Kellner H, Levin L, Jehmlich N, Hofrichter M, Ullrich R (2013) The secretome of Trametes versicolor grown on tomato juice medium and purification of the secreted oxidoreductases including a versatile peroxidase. J Biotechnol 168:15–23

    CAS  PubMed  Google Scholar 

  • Coconi-Linares N, Magaña-Ortíz D, Guzmán-Ortiz DA, Fernández F, Loske AM, Gómez-Lim MA (2014) High-yield production of manganese peroxidase, lignin peroxidase, and versatile peroxidase in Phanerochaete chrysosporium. Appl Microbiol Biotechnol 98:9283–9294

    CAS  PubMed  Google Scholar 

  • Cohen R, Hadar Y, Yarden O (2001) Transcript and activity levels of different Pleurotus ostreatus peroxidases are differentially affected by Mn2+. Environ Microbiol 3:312–322

    CAS  PubMed  Google Scholar 

  • Cohen R, Persky L, Hadar Y (2002a) Lignocellulose affects Mn2+ regulation of peroxidase transcript levels in solid-state culture of Pleurotus ostreatus. Appl Environ Microbiol 68:3156–3158

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cohen R, Persky L, Hadar Y (2002b) Biotechnological applications and potential of wood-degrading mushrooms of the genus Pleurotus. Appl Microbiol Biotechnol 58:582–594

    CAS  PubMed  Google Scholar 

  • Cohen R, Persky L, Hazan-Eitan Z, Yarden O, Hadar Y (2002c) Mn2+ alters peroxidase profiles and lignin degradation by the white-rot fungus Pleurotus ostreatus under different nutritional and growth conditions. Appl Biochem Biotechnol 102:415–429

    PubMed  Google Scholar 

  • Daniel G, Volc J, Kubátová E (1994) Pyranose oxidase, a major source of H2O2 during wood degradation by Phanerochaete chrysosporium, Trametes versicolor, and Oudemansiella mucida. Appl Environ Microbiol 60:2524–2532

    CAS  PubMed Central  PubMed  Google Scholar 

  • Deepalakshmi K, Mirunalini S (2014) Pleurotus ostreatus: an oyster mushroom with nutritional and medicinal properties. J Biochem Tech 5:718–726

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ertan H, Siddiqui KS, Muenchhoff J, Charlton T, Cavicchioli R (2012) Kinetic and thermodynamic characterization of the functional properties of a hybrid versatile peroxidise using isothermal titration calorimetry: insights into manganese peroxidase activation and lignin peroxidase inhibition. Biochimie 94:1221–1231

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Fernández-Fueyo E, Ruiz-Dueñas FJ, Miki Y, Martínez MJ, Hammel KE, Martínez AT (2012) Lignin-degrading peroxidases from genome of selective ligninolytic fungus Ceriporiopsis subvermispora. J Biol Chem 287:16309–16916

    Google Scholar 

  • Fernández-Fueyo E, Ruiz-Dueñas FJ, Martínez MJ, Romero A, Hammel KE, Medrano FJ, Martínez AT (2014a) Ligninolytic peroxidase genes in the oyster mushroom genome: heterologous expression, molecular structure, catalytic and stability properties, and lignin-degrading ability. Biotechnol Biofuels 7:2–23

    PubMed Central  PubMed  Google Scholar 

  • Fernández-Fueyo E, Castanera ER, Ruiz-Dueñas FJ, López-Lucendo MF, Ramírez A, Pisabarro AG, Martínez AT (2014b) Ligninolytic peroxidase gene expression by Pleurotus ostreatus: differential regulation in lignocellulose medium and effect of temperature and pH. Fungal Genet Biol. doi:10.1016/j.fgb.2014.02.003

    PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, John FS, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719

    CAS  PubMed  Google Scholar 

  • Gaskell J, Marty A, Mozuch M, Kersten PJ, Splinter S, Durant B, Sabat G, Azarpira A, Ralph J, Skyba O, Mansfield SD, Blanchette RA, Cullen D (2014) Influence of Populus genotype on gene expression by the wood decay fungus Phanerochaete chrysosporium. Appl Environ Microbiol 80:5828-5835

  • Gasser CA, Hommes G, Schäffer A, Corvini PF-X (2012) Multi-catalysis reactions: new prospects and challenges of biotechnology to valorize lignin. Appl Microbiol Biotechnol 95:1115–1134

    CAS  PubMed  Google Scholar 

  • Giardina P, Palmieri G, Fontanella B, Rivieccio V, Sannia G (2000) Manganese peroxidase isoenzymes produced by Pleurotus ostreatus grown on wood sawdust. Arch Biochem Biophys 376:171–179

    CAS  PubMed  Google Scholar 

  • Golan-Rozen N, Chefetz B, Ben-Ari J, Geva J, Hadar Y (2011) Transformation of the recalcitrant pharmaceutical compound carbamazepine by Pleurotus ostreatus: role of cytochrome P450 monooxygenase and manganese peroxidase. Environ Sci Technol 45:6800–6805

    CAS  PubMed  Google Scholar 

  • Gold MH, Youngs HL, Gelpke MDS (2000) Manganese peroxidase. Met Ions Biol Syst 37:559–586

    CAS  PubMed  Google Scholar 

  • Gutiérrez A, Caramelo L, Prieto A, Martínez MJ, Martínez AT (1994) Anisaldehyde production and aryl-alcohol oxidase and dehydrogenase activities in ligninolytic fungi from the genus Pleurotus. Appl Environ Microbiol 60:1783–1788

    PubMed Central  PubMed  Google Scholar 

  • Haas R, Tsivunchyk O, Steinbach K, Löw EV, Scheibner K, Hofrichter M (2004) Conversion of adamsite (phenarsarzin chloride) by fungal manganese peroxidase. Appl Microbiol Biotechnol 63:564–566

    CAS  PubMed  Google Scholar 

  • Hadar Y, Cullen D (2013) Organopollutant degradation by wood decay basidiomycetes. In: Kempken, F (Ed.) Agricultural applications. The Mycota, 11: 115–141

  • Hammel KE, Cullen D (2008) Role of fungal peroxidases in biological ligninolysis. Curr Opin Plant Biol 11:349–355

    CAS  PubMed  Google Scholar 

  • Heinfling A, Martínez MJ, Martínez AT, Bergbauer M, Szewzyk U (1998) Transformation of industrial dyes by manganese peroxidase from Bjerkandera adusta and Pleurotus eryngii in a manganese-independent reaction. Appl Environ Microbiol 64:2788–2793

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hernández-Ortega A, Ferreira P, Martínez AT (2012) Fungal aryl-alcohol oxidase: a peroxide-producing flavoenzyme involved in lignin degradation. Appl Microbiol Biotechnol 93:1395–1410

    PubMed  Google Scholar 

  • Hildén K, Martínez 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

    PubMed  Google Scholar 

  • Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzym Microb Technol 30:454–466

    CAS  Google Scholar 

  • Hofrichter M, Ullrich R (2014) Oxidations catalyzed by fungal peroxygenases. Currt Opin Chem Biol 19:116–125

    CAS  Google Scholar 

  • Hofrichter M, Ullrich R, Pecyna MJ, Liers C, Lundell T (2010) New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol l87:871–897

    Google Scholar 

  • Ichinose H (2013) Cytochrome P450 of wood-rotting basidiomycetes and biotechnological applications. Biotechnol Appl Biochem 60(1):71–81

    CAS  PubMed  Google Scholar 

  • Irie T, Honda Y, Watanabe T, Kuwahara M (2000) Isolation of cDNA and genome fragments the major manganese peroxidase isozyme from the white rot basidiomycete Pleurotus ostreatus. J Wood Sci 46:230–233

    CAS  Google Scholar 

  • Kamitsuji H, Honda Y, Watanabe T, Kuwahara M (2004) Production and induction of manganese peroxidase isoenzymes in a whit-rot fungus Pleurotus ostreatus. Appl Microbiol Biotechnol 65:287–294

    CAS  PubMed  Google Scholar 

  • Kamitsuji H, Watanabe T, Honda Y, Kuwahara M (2005a) Direct oxidation of polymeric substrate by multifunctional manganese peroxidase isoenzyme from Pleurotus ostreatus without redox mediators. Biochem J 385:387–393

    Google Scholar 

  • Kamitsuji H, Honda Y, Watanabe T, Kuwahara M (2005b) Mn2+ is dispensable for the production of active MnP2 by Pleurotus ostreatus. Biochem Biophys Res Commun 327:871–876

    CAS  PubMed  Google Scholar 

  • Kerem Z, Hadar Y (1995) Effect of manganese on preferential lignin degradation by Pleurotus ostreatus during solid-state fermentation. Appl Environ Microbiol 61:3057–3062

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kersten P, Cullen D (2014) Copper radical oxidases and related extracellular oxidoreductases of wood-decay Agaricomycetes. Fungal Genet Biol. doi:10.1016/j.fgb.2014.05.011

    PubMed  Google Scholar 

  • Kersten PJ, Kirk TK (1987) Involvement of a new enzyme, glyoxal oxidase, in extracellular H2O2 production by Phanerochaete chrysosporium. J Bacteriol 169:2195–2201

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Kirk TK, Farrell RL (1987) Enzymatic ‘combustion’: the microbial degradation of lignin. Annu Rev Microbiol 41:465–505

    CAS  PubMed  Google Scholar 

  • Knop D, Ben-Ari J, Salame TM, Levinson D, Yarden O, Hadar Y (2014) Mn2+-deficiency reveals a key role for the Pleurotus ostreatus versatile peroxidase (VP4) in oxidation of aromatic compounds. Appl Microbiol Biotechnol 98:6795–6804

    CAS  PubMed  Google Scholar 

  • Kofujita H, Asada Y, Kuwahara M (1991) Arkil-aryl cleavage of phenolic β-O-4 lignin substructure model compound by Mn-peroxidase isolated from Pleurotus ostreatus. Mokuzai Gakkaishi 37:555–561

    CAS  Google Scholar 

  • Kuwahara M, Glenn JK, Morgan MA, Gold MH (1984) Separation and characterization of 2 extracellular H2O2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett 169:247–250

    CAS  Google Scholar 

  • Levasseur A, Lomascolo A, Chabrol O, Ruiz-Dueñas FJ, Boukhris-Uzan E, Piumi F, Kües U, Ram AFJ, Murat C, Haon M, Benoit I, Arfi Y, Chevret D, Drula E, Kwon MJ, Gouret P, Lesage-Meessen L, Lombard V, Mariette J, Noirot C, Park J, Patyshakuliyeva A, Sigoillot JC, Wiebenga A, Wösten HAB, Martin F, Coutinho PM, de Vries RP, Martínez AT, Klopp C, Pontarotti P, Henrissat B, Record E (2014) The genome of the white-rot fungus Pycnoporus cinnabarinus: a basidiomycete model with a versatile arsenal for lignocellulosic biomass breakdown. BMC Genomics. doi:10.1186/1471-2164-15-486

    PubMed Central  PubMed  Google Scholar 

  • Liers C, Pecyna MJ, Kellner H, Worrich A, Zorn H, Steffen KT, Hofrichter M, Ullrich R (2013) Substrate oxidation by dye-decolorizing peroxidases (DyPs) from wood- and litter-degrading agaricomycetes compared to other fungal and plant heme-peroxidases. Appl Microbiol Biotechnol 97:5839–5849

    CAS  PubMed  Google Scholar 

  • Martínez AT (2002) Molecular biology and structure-function of lignin-degrading heme peroxidases. Enzym Microb Technol 30:425–444

    Google Scholar 

  • Martínez MJ, Ruiz-Dueñas FJ, Guillén F, Martínez AT (1996a) Purification and catalytic properties of two manganese peroxidase isoenzymes from Pleurotus eryngii. Eur J Biochem 237:424–432

    PubMed  Google Scholar 

  • Martínez MJ, Böckle B, Camarero S, Guillén F, Martínez AT (1996b) 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

    Google Scholar 

  • Morales M, Mate MJ, Romero A, Martínez MJ, Martínez AT, Ruiz-Dueñas FJ (2012) Two oxidation sites for low redox potential substrates: a direct mutagenesis, kinetic, and, crystallographic study on Pleurotus eryngii versatile peroxidase. J Biol Chem 287:41053–41067

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ohm RA, Riley R, Salamov A, Min B, Choi I-G, Grigoriev IV (2014) Genomics of wood-degrading fungi. Fungal Genet Biol 72:82-90

  • Pawlik A, Janusz G, Koszerny J, Małek W, Rogalski J (2012) Genetic diversity of the edible mushroom Pleurotus sp. by amplified fragment length polymorphism. Curr Microbiol 65(4):438–445

    CAS  PubMed Central  PubMed  Google Scholar 

  • Perez J, Jeffries TM (1992) Roles of manganese and organic acid chelators in regulating lignin degradation and biosynthesis of peroxidase by Phanerochaete chrysosporium. Appl Environ Microbiol 58:2402–2409

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pérez-Boada M, Doyle WA, Ruiz-Dueñas FJ, Martínez MJ, Martínez AT, Smith AT (2002) Expression of Pleurotus eryngii versatile peroxidase in Escherichia coli and optimisation of in vitro folding. Enzym Microb Technol 30(4):518–524

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Pezzella C, Autore F, Giardina P, Piscitelli A, Sannia G, Faraco V (2009) The Pleurotus ostreatus laccase multi-gene family: isolation and heterologous expression of new family members. Curr Genet 55:45–57

    CAS  PubMed  Google Scholar 

  • Pezzella C, Lettera V, Piscitelli A, Giardina P, Sannia G (2013) Transcriptional analysis of Pleurotus ostreatus laccase genes. Appl Microbiol Biotechnol 97:705–717

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Poulos TL, Edwards SL, Wariishi H, Gold MH (1993) Crystallographic refinement of lignin peroxidase at 2 A. J Biol Chem 268:4429–4440

    CAS  PubMed  Google Scholar 

  • Rao MA, Scelza R, Acevedo F, Diez MC, Gianfreda L (2014) Enzymes as useful tools for environmental purposes. Chemosphere 107:145–162

    CAS  PubMed  Google Scholar 

  • Riley R, Salamov AA, Brown DW, Nagy LG, Floudas D, Held BW, Levasseur A, Lombard V, Morin E, Otillar R, Lindquist EA, Sun H, LaButti KM, Schmutz J, Jabbour D, Luo H, Baker SE, Pisabarro AG, Walton JD, Blanchette RA, Henrissat B, Martin F, Cullen D, Hibbett DS, Grigoriev IV (2014) Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci U S A 111:9923–9928

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ruiz-Dueñas FJ, Guillén F, Camarero S, Pérez-Boada M, Martínez MJ, Martínez AT (1999) Regulation of peroxidase transcript levels in liquid cultures of the ligninolytic fungus Pleurotus eryngii. Appl Environ Microbiol 65:4458–4463

    PubMed Central  PubMed  Google Scholar 

  • Ruiz-Dueñas FJ, Morales M, Pérez-Boada M, Choinowski T, Martínez MJ, Piontek K, Martínez AT (2007) Manganese oxidation site in Pleurotus eryngii versatile peroxidase: a site-directed mutagenesis, kinetic, and crystallographic study. Biochemistry 46:66–77

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Ruiz-Dueñas FJ, Fernández E, Martínez MJ, Martínez AT (2011) Pleurotus ostreatus heme peroxidases: an in silico analysis from the genome sequence to the enzyme molecular structure. C R Biolog 334:795–805

    Google Scholar 

  • Ruiz-Dueñas FJ, Lundell T, Floudas D, Nagy LG, Barrasa JM, Hibbett DS, Martínez AT (2013) Lignin-degrading peroxidases in Polyporales: an evolutionary survey based on 10 sequenced genomes. Mycologia 105:1424–1444

    Google Scholar 

  • Rüttimann-Johnson C, Salas L, Vicuna R, Kirk TK (1993) Extracellular enzyme production and synthetic lignin mineralization by Ceriporiopsis subvermispora. Appl Environ Microbiol 59:1792–1797

    PubMed Central  PubMed  Google Scholar 

  • Salame TM, Yarden O, Hadar Y (2010) Pleurotus ostreatus manganese-dependent peroxidase silencing impairs decolourization of Orange II. Microb Biotechnol 3:93–106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Salame TM, Ziv C, Hadar Y, Yarden O (2011) RNAi as a potential tool for biotechnological applications in fungi. Appl Microbiol Biotechnol 89:501–512

    CAS  PubMed  Google Scholar 

  • Salame TM, Knop D, Tal D, Levinson D, Yarden O, Hadar Y (2012a) Predominance of a versatile-peroxidase-encoding gene, mnp4, as demonstrated by gene replacement via a gene targeting system for Pleurotus ostreatus. Appl Environ Microbiol 78:5341–5352

    CAS  PubMed Central  PubMed  Google Scholar 

  • Salame TM, Knop D, Levinson D, Mabjeesh SJ, Yarden O, Hadar Y (2012b) Release of Pleurotus ostreatus versatile peroxidase from Mn2+ repression enhances anthropogenic and natural substrate degradation. PLoS ONE 7:e52446

    CAS  PubMed Central  PubMed  Google Scholar 

  • Salame TM, Knop D, Levinson D, Mabjeesh SJ, Yarden O, Hadar Y (2013) Redundancy among manganese-peroxidases in Pleurotus ostreatus. Appl Environ Microbiol 79:2405–2415

    CAS  PubMed Central  PubMed  Google Scholar 

  • Salame TM, Knop D, Levinson D, Mabjeesh SJ, Yarden O, Hadar Y (2014) Inactivation of a Pleurotus ostreatus versatile peroxidase-encoding gene (mnp2) results in reduced lignin degradation. Environ Microbiol 16:265–277

    CAS  PubMed  Google Scholar 

  • Salvachúa D, Prieto A, Mattinen ML, Tamminen T, Liitiä T, Lille M, Willför S, Martínez AT, Martínez MJ, Faulds CB (2013) Versatile peroxidase as a valuable tool for generating new biomolecules by homogeneous and heterogeneous cross-linking Enzyme. Microb Technol 52:303–311

    Google Scholar 

  • Sanchez C (2010) Cultivation of Pleurotus ostreatus and other edible mushrooms. Appl Microbiol Biotechnol 85:1321–1337

    CAS  PubMed  Google Scholar 

  • Sarkar S, Martínez AT, Martínez MJ (1997) Biochemical and molecular characterization of a manganese peroxidase isoenzyme from Pleurotus ostreatus. BBA-Protein Struct Mol 1339:23–30

    CAS  Google Scholar 

  • Schüttmann I, Bouws H, Szweda RT, Suckow M, Czermak P, Zorn H (2014) Induction, characterization, and heterologous expression of a carotenoid degrading versatile peroxidase from Pleurotus sapidus. J Mol Catal B Enzym 103:79–84

    Google Scholar 

  • Shaw PD, Hager LP (1959) Biological chlorination. III. beta-Ketoadipate chlorinase: a soluble enzyme system. J Biol Chem 234:2565–2569

    CAS  PubMed  Google Scholar 

  • Shnyreva AA, Sivolapova AB, Shnyreva AV (2012) The commercially cultivated edible oyster mushrooms Pleurotus sajor-caju and P. pulmonarius are two separated species, similar in morphology but reproductively isolated. Russ J Genet 48:1080–1088

    CAS  Google Scholar 

  • Singh AP, Singh T (2014) Biotechnological applications of wood-rotting fungi: a review. Biomass Bioenergy 62:198–206

    CAS  Google Scholar 

  • Smith AT, Veitch NC (1998) Substrate binding and catalysis in heme peroxidases. Curr Opin Chem Biol 2:269–278

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Solís M, Solís A, Pérez HI, Manjarrez N, Flores M (2012) Microbial decolouration of azo dyes: a review. Process Biochem 47:1723–1748

    Google Scholar 

  • Songulashvili G, Elisashvili V, Wasser SP, Nevo E, Hadar Y (2007) Basidiomycetes laccase and manganese peroxidase activity in submerged fermentation of food industry wastes. Enzym Microb Technol 41:57–61

    CAS  Google Scholar 

  • Stajić M, Persky L, Friesem D, Hadar Y, Wasser SP, Eviatar N, Vukojevi J (2006) Effect of different carbon and nitrogen sources on laccase and peroxidases production by selected Pleurotus species. Enzym Microbiol Technol 38:65–73

    Google Scholar 

  • Stajić M, Vukojević J, Duletić-Laušević S (2009) Biology of Pleurotus eryngii and role in biotechnological processes: a review. Crit Rev Biotechnol 29:55–66

    PubMed  Google Scholar 

  • Sugano Y (2009) DyP-type peroxidases comprise a novel heme peroxidase family. Cell Mol Life Sci 66:1387–1403

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 10:2731–2739

    Google Scholar 

  • Touahar IE, Haroune I, Ba S, Bellenger JP, Cabana H (2014) Characterization of combined cross-linked enzyme aggregates from laccase, versatile peroxidase and glucose oxidase, and their utilization for the elimination of pharmaceuticals. Sci Total Environ 481:90–99

    CAS  PubMed  Google Scholar 

  • Tsukihara T, Honda Y, Watanabe T, Watanabe T (2006a) Exclusive overproduction of recombinant versatile peroxidase MnP2 by genetically modified white rot fungus, Pleurotus ostreatus. J Biotechnol 126:431–439

    CAS  PubMed  Google Scholar 

  • Tsukihara T, Honda Y, Watanabe T, Watanabe T (2006b) Molecular breeding of white rot fungus Pleurotus ostreatus by homologous expression of its versatile peroxidase MnP2. Appl Microbiol Biotechnol 71:114–120

    CAS  PubMed  Google Scholar 

  • Tsukihara T, Honda Y, Sakai R, Watanabe T (2008) Mechanism for oxidation of high-molecular-weight substrates by a fungal versatile peroxidase, MnP2. Appl Environ Microbiol 74:2873–2881

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vásquez C, Anderson D, Oyarzún M, Carvajal A, Palma C (2014) Method for the stabilization and immobilization of enzymatic extracts and its application to the decolorization of textile dyes. Biotechnol Lett 36:1999–2010

    PubMed  Google Scholar 

  • Vilgalys R, Smith A, Sun BL, Miller OK Jr (1993) Intersterility groups in the Pleurotus ostreatus complex from the continental United States and adjacent Canada. Can J Bot 71:113–128

    Google Scholar 

  • Wariishi H, Gold MH (1990) Lignin peroxidase compound III. Mechanism of formation and decomposition. J Biol Chem 265:2070–2077

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Yao Y, Sakamoto T, Honda Y, Kagotani Y, Izumitsu K, Suzuki K, Irie T (2013) The white-rot fungus Pleurotus ostreatus transformant overproduced intracellular cAMP and laccase. Biosci Biotechnol Biochem 77:2309–2311

    CAS  PubMed  Google Scholar 

  • Zervakis G, Balis C (1996) A pluralistic approach in the study of Pleurotus species with emphasis on compatibility and physiology of the European morphotaxa. Mycol Res 100:717–731

    Google Scholar 

  • Zhao X, Lu Y, Phillips DR, Hwang H-M, Hardin IR (2007) Study of biodegradation products from azo dyes in fungal degradation by capillary electrophoresis/electrospray mass spectrometry. J Chromatogr A 1159:217–224

    CAS  PubMed  Google Scholar 

  • Zorn H, Peters T, Nimtz M, Berger RG (2005) The secretome of Pleurotus sapidus. Proteomics 5:4832–4838

    CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by grants from US–Israel binational Fund (BSF) and The Israel Science foundation (ISF).

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  1. Department of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 76100, Israel

    Doriv Knop, Oded Yarden & Yitzhak Hadar

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  1. Doriv Knop
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  2. Oded Yarden
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  3. Yitzhak Hadar
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Correspondence to Yitzhak Hadar.

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Knop, D., Yarden, O. & Hadar, Y. The ligninolytic peroxidases in the genus Pleurotus: divergence in activities, expression, and potential applications. Appl Microbiol Biotechnol 99, 1025–1038 (2015). https://doi.org/10.1007/s00253-014-6256-8

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  • DOI: https://doi.org/10.1007/s00253-014-6256-8

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