Microbial enzyme systems for lignin degradation and their transcriptional regulation

Abstract

Lignocellulosic biomass is the most abundant renewable resource in nature and has received considerable attention as one of the most promising alternatives to oil resources for the provision of energy and certain raw materials. The phenolic polymer lignin is the second most abundant constituent of this biomass resource and has been shown to have the potential to be converted into industrially important aromatic chemicals after degradation. However, due to its chemical and structural nature, it exhibits high resistance toward mechanical, chemical, and biological degradation, and this causes a major obstacle for achieving efficient conversion of lignocellulosic biomass. In nature, lignin-degrading microorganisms have evolved unique extracellular enzyme systems to decompose lignin using radical mediated oxidative reactions. These microorganisms produce a set of different combinations of enzymes with multiple isozymes and isoforms by responding to various environmental stimuli such as nutrient availability, oxygen concentration and temperature, which are thought to enable effective decomposition of the lignin in lignocellulosic biomass. In this review, we present an overview of the microbial ligninolytic enzyme systems including general molecular aspects, structural features, and systematic differences in each microorganism. We also describe the gene expression pattern and the transcriptional regulation mechanisms of each ligninolytic enzyme with current data.

Keywords

lignocellulose biorefinery / lignin degradation / lignin peroxidases / manganese peroxidases / versatile peroxidases / laccases

References

[1] Adler E (1977). Lignin chemistry—past, present and future. Wood Sci Technol, 11(3): 169–218

[2] Ahmad M, Roberts J N, Hardiman E M, Singh R, Eltis L D, Bugg T D (2011). Identification of DypB from Rhodococcus jostii RHA1 as a lignin peroxidase. Biochemistry, 50(23): 5096–5107

[3] Ahmad M, Taylor C R, Pink D, Burton K, Eastwood D, Bending G D, Bugg T D (2010). Development of novel assays for lignin degradation: comparative analysis of bacterial and fungal lignin degraders. Mol Biosyst, 6(5): 815–821

[4] Akin D E, Morrison Iii W H, Rigsby L L, Gamble G R, Sethuraman A, Eriksson K E L (1996). Biological delignification of plant components by the white rot fungi Ceriporiopsis subvermispora and Cyathus stercoreus. Anim Feed Sci Technol, 63(1–4): 305–321

[5] Alvarez J M, Canessa P, Mancilla R A, Polanco R, Santibáñez P A, Vicuña R (2009). Expression of genes encoding laccase and manganese-dependent peroxidase in the fungus Ceriporiopsis subvermispora is mediated by an ACE1-like copper-fist transcription factor. Fungal Genet Biol, 46(1): 104–111

[6] Andreu G, Vidal T (2011). Effects of laccase-natural mediator systems on kenaf pulp. Bioresour Technol, 102(10): 5932–5937

[7] Antoni D, Zverlov V V, Schwarz W H (2007). Biofuels from microbes. Appl Microbiol Biotechnol, 77(1): 23–35

[8] Arantes V, Jellison J, Goodell B (2012). Peculiarities of brown-rot fungi and biochemical Fenton reaction with regard to their potential as a model for bioprocessing biomass. Appl Microbiol Biotechnol, 94(2): 323–338

[9] Asgher M, Bhatti H N, Ashraf M, Legge R L (2008). Recent developments in biodegradation of industrial pollutants by white rot fungi and their enzyme system. Biodegradation, 19(6): 771–783

[10] Ausec L, Zakrzewski M, Goesmann A, Schlüter A, Mandic-Mulec I (2011). Bioinformatic analysis reveals high diversity of bacterial genes for laccase-like enzymes. PLoS One, 6(10): e25724

[11] Azadi P, Inderwildi O R, Farnood R, King D A (2013). Liquid fuels, hydrogen and chemicals from lignin: A critical review. Renew Sustain Energy Rev, 21: 506–523

[12] Bajpai P (2004). Biological bleaching of chemical pulps. Crit Rev Biotechnol, 24(1): 1–58

[13] Bajpai P, Anand A, Bajpai P K (2006). Bleaching with lignin-oxidizing enzymes. Biotechnol Annu Rev, 12: 349–378

[14] Balakshin Mikhail Y, Capanema Ewellyn A, Chang H (2007). MWL fraction with a high concentration of lignin-carbohydrate linkages: Isolation and 2D NMR spectroscopic analysis. Holzforschung, 61(1): 1–7

[15] Baldrian P (2006). Fungal laccases- occurrence and properties. FEMS Microbiol Rev, 30(2): 215–242

[16] Banci L, Camarero S, Martínez A T, Martínez M J, Pérez-Boada M, Pierattelli R, Ruiz-Dueñas F J (2003). NMR study of manganese(II) binding by a new versatile peroxidase from the white-rot fungus Pleurotus eryngii. J Biol Inorg Chem, 8(7): 751–760

[17] Bao W, Fukushima Y, Jensen K A Jr, Moen M A, Hammel K E (1994). Oxidative degradation of non-phenolic lignin during lipid peroxidation by fungal manganese peroxidase. FEBS Lett, 354(3): 297–300

[18] Beedlow P A, Tingey D T, Phillips D L, Hogsett W E, Olszyk D M (2004). Rising atmospheric CO₂ and carbon sequestration in forests. Front Ecol Environ, 2: 315–322

[19] Belinky P A, Flikshtein N, Lechenko S, Gepstein S, Dosoretz C G (2003). Reactive oxygen species and induction of lignin peroxidase in Phanerochaete chrysosporium. Appl Environ Microbiol, 69(11): 6500–6506

[20] Bindoff N L, Stott P A, AchutaRao K M, Allen M R, Gillett N, Gutzler D, Hansingo K, Hegerl G, Hu Y, Jain S, Mokhov I I, Overland J, Perlwitz J, Sebbari R, Zhang X (2013). Detection and Attribution of Climate Change: from Global to Regional. In: Stocker T F, Qin D, Plattner G K, Tignor M, Allen S K, Boschung J, Nauels A, Xia Y, Bex V, Midgley P M (eds.) . Climate Change 2013: The Physical Science Basis Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, United Kingdom and New York, NY, USA, Cambridge University Press, 867–952

[21] Blanchette R A (1995). Degradation of the lignocellulose complex in wood. Can J Bot, 73(S1): 999–1010

[22] Blanchette Robert A, Burnes Todd A, Eerdmans Marjorie M, Akhtar M (1992). Evaluating isolates of Phanerochaete chrysosporium and Ceriporiopsis subvermispora for use in biological pulping processes. Holzforschung, 46(2): 109–116

[23] Boerjan W, Ralph J, Baucher M (2003). Lignin biosynthesis. Annu Rev Plant Biol, 54(1): 519–546

[24] Bogan B W, Schoenike B, Lamar R T, Cullen D (1996). Expression of lip genes during growth in soil and oxidation of anthracene by Phanerochaete chrysosporium. Appl Environ Microbiol, 62(10): 3697–3703

[25] Bourbonnais R, Paice M G (1990). Oxidation of non-phenolic substrates. An expanded role for laccase in lignin biodegradation. FEBS Lett, 267(1): 99–102

[26] Bozell J J, Petersen G R (2010). Technology development for the production of biobased products from biorefinery carbohydrates—the US Department of Energy’s “Top 10” revisited. Green Chem, 12(4): 539

[27] Brown J A, Li D, Alic M, Gold M H (1993). Heat Shock induction of manganese peroxidase gene transcription in Phanerochaete chrysosporium. Appl Environ Microbiol, 59(12): 4295–4299

[28] Brown M E, Barros T, Chang M C (2012). Identification and characterization of a multifunctional dye peroxidase from a lignin-reactive bacterium. ACS Chem Biol, 7(12): 2074–2081

[29] Bugg T D, Ahmad M, Hardiman E M, Rahmanpour R (2011a). Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep, 28(12): 1883–1896

[30] Bugg T D, Ahmad M, Hardiman E M, Singh R (2011b). The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol, 22(3): 394–400

[31] Call H P, Mücke I (1997). History, overview and applications of mediated lignolytic systems, especially laccase-mediator-systems (Lignozym®-process). J Biotechnol, 53(2–3): 163–202

[32] Camarero S, Ibarra D, Martínez M J, Martínez A T (2005). Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl Environ Microbiol, 71(4): 1775–1784

[33] Cañas A I, Camarero S (2010). Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv, 28(6): 694–705

[34] Canessa P, Alvarez J M, Polanco R, Bull P, Vicuña R (2008). The copper-dependent ACE1 transcription factor activates the transcription of the mco1 gene from the basidiomycete Phanerochaete chrysosporium. Microbiology, 154(Pt 2): 491–499

[35] Chen F, Dixon R A (2007). Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol, 25(7): 759–761

[36] Choinowski T, Blodig W, Winterhalter K H, Piontek K (1999). The crystal structure of lignin peroxidase at 1.70 A resolution reveals a hydroxy group on the cbeta of tryptophan 171: a novel radical site formed during the redox cycle. J Mol Biol, 286(3): 809–827

[37] Claus H (2003). Laccases and their occurrence in prokaryotes. Arch Microbiol, 179(3): 145–150

[38] Claus H (2004). Laccases: structure, reactions, distribution. Micron, 35(1–2): 93–96

[39] Cohen R, Hadar Y, Yarden O (2001). Transcript and activity levels of different Pleurotus ostreatus peroxidases are differentially affected by Mn²⁺. Environ Microbiol, 3(5): 312–322

[40] Cohen R, Yarden O, Hadar Y (2002). Lignocellulose affects Mn²⁺ regulation of peroxidase transcript levels in solid-state cultures of Pleurotus ostreatus. Appl Environ Microbiol, 68(6): 3156–3158

[41] Colao M Ch, Garzillo A M, Buonocore V, Schiesser A, Ruzzi M (2003). Primary structure and transcription analysis of a laccase-encoding gene from the basidiomycete Trametes trogii. Appl Microbiol Biotechnol, 63(2): 153–158

[42] Collins P J, Dobson A (1997). Regulation of laccase gene transcription in trametes versicolor. Appl Environ Microbiol, 63(9): 3444–3450

[43] Collins P J, O’Brien M M, Dobson A D (1999). Cloning and characterization of a cDNA encoding a novel extracellular peroxidase from trametes versicolor. Appl Environ Microbiol, 65(3): 1343–1347

[44] Colpa D I, Fraaije M W, van Bloois E (2014). DyP-type peroxidases: a promising and versatile class of enzymes. J Ind Microbiol Biotechnol, 41(1): 1–7

[45] Conesa A, Punt P J, van den Hondel C A (2002). Fungal peroxidases: molecular aspects and applications. J Biotechnol, 93(2): 143–158

[46] Crestini C, Crucianelli M, Orlandi M, Saladino R (2010). Oxidative strategies in lignin chemistry: A new environmental friendly approach for the functionalisation of lignin and lignocellulosic fibers. Catal Today, 156(1–2): 8–22

[47] Crestini C, Melone F, Sette M, Saladino R (2011). Milled wood lignin: a linear oligomer. Biomacromolecules, 12(11): 3928–3935

[48] Cullen D (1997). Recent advances on the molecular genetics of ligninolytic fungi. J Biotechnol, 53(2-3): 273–289

[49] Dhawale S S, Lane A C (1993). Compilation of sequence-specific DNA-binding proteins implicated in transcriptional control in fungi. Nucleic Acids Res, 21(24): 5537–5546

[50] Doherty W O S, Mousavioun P, Fellows C M (2011). Value-adding to cellulosic ethanol: Lignin polymers. Ind Crops Prod, 33(2): 259–276

[51] Dooley D M, Rawlings J, Dawson J H, Stephens P J, Andreasson L E, Malmstrom B G, Gray H B (1979). Spectroscopic studies of Rhus vernicifera and Polyporus versicolor laccase. Electronic structures of the copper sites. J Am Chem Soc, 101(17): 5038–5046

[52] Dowzer C E, Kelly J M (1991). Analysis of the creA gene, a regulator of carbon catabolite repression in Aspergillus nidulans. Mol Cell Biol, 11(11): 5701–5709

[53] Doyle W A, Blodig W, Veitch N C, Piontek K, Smith A T (1998). Two substrate interaction sites in lignin peroxidase revealed by site-directed mutagenesis. Biochemistry, 37(43): 15097–15105

[54] Drysdale M R, Kolze S E, Kelly J M (1993). The Aspergillus niger carbon catabolite repressor encoding gene, creA. Gene, 130(2): 241–245

[55] Dunford H B (1999). Heme peroxidases, New York, Wiley

[56] Dusselier M, Mascal M, Sels B F (2014). Top chemical opportunities from carbohydrate biomass: A chemist’s view of the biorefinery. Top Curr Chem, 353: 1–40

[57] Dwivedi U N, Singh P, Pandey V P, Kumar A (2011). Structure–function relationship among bacterial, fungal and plant laccases. J Mol Catal, B Enzym, 68: 117–128

[58] Edwards S L, Raag R, Wariishi H, Gold M H, Poulos T L (1993). Crystal structure of lignin peroxidase. Proc Natl Acad Sci U S A, 90(2): 750–754

[59] Eggert C, Temp U, Dean J F D, Eriksson K E L (1996). A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase. FEBS Lett, 391(1–2): 144–148

[60] Eggert C, Temp U, Eriksson K E (1997). Laccase is essential for lignin degradation by the white-rot fungus Pycnoporus cinnabarinus. FEBS Lett, 407(1): 89–92

[61] Elisashvili V, Kachlishvili E (2009). Physiological regulation of laccase and manganese peroxidase production by white-rot Basidiomycetes. J Biotechnol, 144(1): 37–42

[62] Enguita F J, Martins L O, Henriques A O, Carrondo M A (2003). Crystal structure of a bacterial endospore coat component. A laccase with enhanced thermostability properties. J Biol Chem, 278(21): 19416–19425

[63] Eriksson K E L B R A, Ander P (1990). Microbial and Enzymatic Degradation of Wood and Wood Components. Berlin, Springer, 1–72

[64] Ertan H, Siddiqui K S, Muenchhoff J, Charlton T, Cavicchioli R (2012). Kinetic and thermodynamic characterization of the functional properties of a hybrid versatile peroxidase using isothermal titration calorimetry: Insight into manganese peroxidase activation and lignin peroxidase inhibition. Biochimie, 94(5): 1221–1231

[65] Fackler K, Gradinger C, Hinterstoisser B, Messner K, Schwanninger M (2006). Lignin degradation by white rot fungi on spruce wood shavings during short-time solid-state fermentations monitored by near infrared spectroscopy. Enzyme Microb Technol, 39(7): 1476–1483

[66] Faraco V, Giardina P, Sannia G (2003). Metal-responsive elements in Pleurotus ostreatus laccase gene promoters. Microbiology, 149(Pt 8): 2155–2162

[67] Faraco V, Piscitelli A, Sannia G, Giardina P (2006). Identification of a new member of the dye-decolorizing peroxidase family from Pleurotus ostreatus. World J Microb Biot, 23(6): 889–893

[68] Fernández-Fueyo E, Castanera R, Ruiz-Dueñas F J, López-Lucendo M F, Ramírez L, Pisabarro A G, Martínez A T (2014a). Ligninolytic peroxidase gene expression by Pleurotus ostreatus: Differential regulation in lignocellulose medium and effect of temperature and pH. Fungal Genet Biol, (In press)

[69] Fernandez-Fueyo E, Ruiz-Dueñas F J, Ferreira P, Floudas D, Hibbett D S, Canessa P, Larrondo L F, James T Y, Seelenfreund D, Lobos S, Polanco R, Tello M, Honda Y, Watanabe T, Watanabe T, Ryu J S, Kubicek C P, Schmoll M, Gaskell J, Hammel K E, St John F J, Vanden Wymelenberg A, Sabat G, Splinter BonDurant S, Syed K, Yadav J S, Doddapaneni H, Subramanian V, Lavín J L, Oguiza J A, Perez G, Pisabarro A G, Ramirez L, Santoyo F, Master E, Coutinho P M, Henrissat B, Lombard V, Magnuson J K, Kües U, Hori C, Igarashi K, Samejima M, Held B W, Barry K W, LaButti K M, Lapidus A, Lindquist E A, Lucas S M, Riley R, Salamov A A, Hoffmeister D, Schwenk D, Hadar Y, Yarden O, de Vries R P, Wiebenga A, Stenlid J, Eastwood D, Grigoriev I V, Berka R M, Blanchette R A, Kersten P, Martinez A T, Vicuna R, Cullen D (2012). Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc Natl Acad Sci U S A, 109(14): 5458–5463

[70] Fernández-Fueyo E, Ruiz-Dueñas F J, Martínez M J, Romero A, Hammel K E, Medrano F J, Martínez A T (2014b). Ligninolytic peroxidase genes in the oyster mushroom genome: heterologous expression, molecular structure, catalytic and stability properties, and lignin-degrading ability. Biotechnol Biofuels, 7(1): 2

[71] Fillat A, Colom J F, Vidal T (2010). A new approach to the biobleaching of flax pulp with laccase using natural mediators. Bioresour Technol, 101(11): 4104–4110

[72] FitzPatrick M, Champagne P, Cunningham M F, Whitney R A (2010). A biorefinery processing perspective: treatment of lignocellulosic materials for the production of value-added products. Bioresour Technol, 101(23): 8915–8922

[73] Floudas D, Binder M, Riley R, Barry K, Blanchette R A, Henrissat B, Martínez A T, Otillar R, Spatafora J W, Yadav J S, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho P M, de Vries R P, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens J A, Kallen N, Kersten P, Kohler A, Kües U, Kumar T K, Kuo A, LaButti K, Larrondo L F, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin D J, Morgenstern I, Morin E, Murat C, Nagy L G, Nolan M, Ohm R A, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas F J, Sabat G, Salamov A, Samejima M, Schmutz J, Slot J C, St John F, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood D C, Martin F, Cullen D, Grigoriev I V, Hibbett D S (2012). The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science, 336(6089): 1715–1719

[74] Galhaup C, Goller S, Peterbauer C K, Strauss J, Haltrich D (2002). Characterization of the major laccase isoenzyme from Trametes pubescens and regulation of its synthesis by metal ions. Microbiology, 148(Pt 7): 2159–2169

[75] Galliano H, Gas G, Seris J L, Boudet A M (1991). Lignin degradation by Rigidoporus lignosus involves synergistic action of two oxidizing enzymes: Mn peroxidase and laccase. Enzyme Microb Technol, 13(6): 478–482

[76] Gardner K H, Blackwell J (1974). The structure of native cellulose. Biopolymers, 13(10): 1975–2001

[77] Gaskell J, Stewart P, Kersten P J, Covert S F, Reiser J, Cullen D (1994). Establishment of genetic linkage by allele-specific polymerase chain reaction: application to the lignin peroxidase gene family of Phanerochaete chrysosporium. Biotechnology (N Y), 12(13): 1372–1375

[78] Gasser C A, Hommes G, Schäffer A, Corvini P F (2012). Multi-catalysis reactions: new prospects and challenges of biotechnology to valorize lignin. Appl Microbiol Biotechnol, 95(5): 1115–1134

[79] Gianfreda L, Xu F, Bollag J M (1999). Laccases: A useful group of oxidoreductive enzymes. Bioremediat J, 3(1): 1–25

[80] Giardina P, Faraco V, Pezzella C, Piscitelli A, Vanhulle S, Sannia G (2010). Laccases: a never-ending story. Cell Mol Life Sci, 67(3): 369–385

[81] Gilbertson R L (1980). Wood-rotting fungi of North-America. Mycologia, 72(1): 1–49

[82] Glenn J K, Akileswaran L, Gold M H (1986). Mn(II) oxidation is the principal function of the extracellular Mn-peroxidase from Phanerochaete chrysosporium. Arch Biochem Biophys, 251(2): 688–696

[83] Glenn J K, Gold M H (1985). Purification and characterization of an extracellular Mn(II)-dependent peroxidase from the lignin-degrading basidiomycete, Phanerochaete chrysosporium. Arch Biochem Biophys, 242(2): 329–341

[84] Goblirsch B, Kurker R C, Streit B R, Wilmot C M, DuBois J L (2011). Chlorite dismutases, DyPs, and EfeB: 3 microbial heme enzyme families comprise the CDE structural superfamily. J Mol Biol, 408(3): 379–398

[85] Godfrey B J, Mayfield M B, Brown J A, Gold M H (1990). Characterization of a gene encoding a manganese peroxidase from Phanerochaete chrysosporium. Gene, 93(1): 119–124

[86] Gold M H, Alic M (1993). Molecular biology of the lignin-degrading basidiomycete Phanerochaete chrysosporium. Microbiol Rev, 57(3): 605–622

[87] Gold M H, Kuwahara M, Chiu A A, Glenn J K (1984). Purification and characterization of an extracellular H₂O₂-requiring diarylpropane oxygenase from the white rot basidiomycete, Phanerochaete chrysosporium. Arch Biochem Biophys, 234(2): 353–362

[88] Golovleva L A, Leontievsky A A, Maltseva O V, Myasoedova N M (1993). Ligninolytic enzymes of the fungus Panus tigrinus 8⁄18: Biosynthesis, purification and properties. J Biotechnol, 30(1): 71–77

[89] Goodell B, Jellison J, Liu J, Daniel G, Paszczynski A, Fekete F, Krishnamurthy S, Jun L, Xu G (1997). Low molecular weight chelators and phenolic compounds isolated from wood decay fungi and their role in the fungal biodegradation of wood. J Biotechnol, 53(2–3): 133–162

[90] Guillén F, Martínez A T, Martínez M J (1992). Substrate specificity and properties of the aryl-alcohol oxidase from the ligninolytic fungus Pleurotus eryngii. Eur J Biochem, 209(2): 603–611

[91] Gupta R, Mehta G, Khasa Y P, Kuhad R C (2011). Fungal delignification of lignocellulosic biomass improves the saccharification of cellulosics. Biodegradation, 22(4): 797–804

[92] Gutiérrez A, del Río J C, Martínez-Iñigo M J, Martínez M J, Martínez A T (2002). Production of new unsaturated lipids during wood decay by ligninolytic basidiomycetes. Appl Environ Microbiol, 68(3): 1344–1350

[93] Hahn-Hägerdal B, Galbe M, Gorwa-Grauslund M F, Lidén G, Zacchi G (2006). Bio-ethanol—the fuel of tomorrow from the residues of today. Trends Biotechnol, 24(12): 549–556

[94] Hakala T K, Hildén K, Maijala P, Olsson C, Hatakka A (2006). Differential regulation of manganese peroxidases and characterization of two variable MnP encoding genes in the white-rot fungus Physisporinus rivulosus. Appl Microbiol Biotechnol, 73(4): 839–849

[95] Hamelinck C N, Hooijdonk G, Faaij A P C (2005). Ethanol from lignocellulosic biomass: techno-economic performance in short-, middle- and long-term. Biomass Bioenergy, 28(4): 384–410

[96] Hammel K E, Jensen K A Jr, Mozuch M D, Landucci L L, Tien M, Pease E A (1993). Ligninolysis by a purified lignin peroxidase. J Biol Chem, 268(17): 12274–12281

[97] Hatakka A (2001) Biodegradation of Lignin. In: Hofrichter M,Steinbuchel A (eds.). (ed) Biopolymers, Wiley-VCH Verlag GmbH & Co. KGaA

[98] Hatti-Kaul R, Törnvall U, Gustafsson L, Börjesson P (2007). Industrial biotechnology for the production of bio-based chemicals—a cradle-to-grave perspective. Trends Biotechnol, 25(3): 119–124

[99] Heinfling A, Ruiz-Dueñas F J, Martínez M J, Bergbauer M, Szewzyk U, Martínez A T (1998). A study on reducing substrates of manganese-oxidizing peroxidases from Pleurotus eryngii and Bjerkandera adusta. FEBS Lett, 428(3): 141–146

[100] Hildén K, Mäkelä M R, Steffen K T, Hofrichter M, Hatakka A, Archer D B, Lundell T K (2014). Biochemical and molecular characterization of an atypical manganese peroxidase of the litter-decomposing fungus Agrocybe praecox. Fungal Genet Biol, (In press)

[101] Hildén K, Martinez A T, 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(5): 403–419

[102] Himmel M E, Ding S Y, Johnson D K, Adney W S, Nimlos M R, Brady J W, Foust T D (2007). Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science, 315(5813): 804–807

[103] Holzbaur E L, Andrawis A, Tien M (1988). Structure and regulation of a lignin peroxidase gene from Phanerochaete chrysosporium. Biochem Biophys Res Commun, 155(2): 626–633

[104] Hon D S (1994). Cellulose: a random walk along its historical path. Cellulose, 1(1): 1–25

[105] Husain M, Husain Q (2007). Applications of redox mediators in the treatment of organic pollutants by using oxidoreductive enzymes: A Review. Crit Rev Environ Sci Technol, 38(1): 1–42

[106] Janusz G, Kucharzyk K H, Pawlik A, Staszczak M, Paszczynski A J (2013). Fungal laccase, manganese peroxidase and lignin peroxidase: gene expression and regulation. Enzyme Microb Technol, 52(1): 1–12

[107] Jeffries T W, Choi S, Kirk T K (1981). Nutritional regulation of lignin degradation by Phanerochaete chrysosporium. Appl Environ Microbiol, 42(2): 290–296

[108] Johansson T, Nyman P O, Cullen D (2002). Differential regulation of mnp2, a new manganese peroxidase-encoding gene from the ligninolytic fungus Trametes versicolor PRL 572. Appl Environ Microbiol, 68(4): 2077–2080

[109] Kamitsuji H, Honda Y, Watanabe T, Kuwahara M (2005). Mn(2+) is dispensable for the production of active MnP2 by Pleurotus ostreatus. Biochem Biophys Res Commun, 327(3): 871–876

[110] Kamm B, Kamm M (2004). Principles of biorefineries. Appl Microbiol Biotechnol, 64(2): 137–145

[111] Kersten P, Cullen D (2007). Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium. Fungal Genet Biol, 44(2): 77–87

[112] Kersten P, Cullen D (2014). Copper radical oxidases and related extracellular oxidoreductases of wood-decay Agaricomycetes. Fungal Genet Biol, (In press)

[113] Kersten P J (1990). Glyoxal oxidase of Phanerochaete chrysosporium: its characterization and activation by lignin peroxidase. Proc Natl Acad Sci U S A, 87(8): 2936–2940

[114] Kersten P J, Kirk T K (1987). Involvement of a new enzyme, glyoxal oxidase, in extracellular H₂O₂ production by Phanerochaete chrysosporium. J Bacteriol, 169(5): 2195–2201

[115] Kim S J, 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(6): 601–607

[116] Kim S J, Shoda M (1999). Purification and characterization of a novel peroxidase from Geotrichum candidum dec 1 involved in decolorization of dyes. Appl Environ Microbiol, 65(3): 1029–1035

[117] Kim Y, Yeo S, Kum J, Song H G, Choi H T (2005). Cloning of a manganese peroxidase cDNA gene repressed by manganese in Trametes versicolor. J Microbiol, 43(6): 569–571

[118] Kirk T K, Croan S, Tien M, Murtagh K E, Farrell R L (1986). Production of multiple ligninases by Phanerochaete chrysosporium: effect of selected growth conditions and use of a mutant strain. Enzyme Microb Technol, 8(1): 27–32

[119] Kirk T K, Farrell R L (1987). Enzymatic “combustion”: the microbial degradation of lignin. Annu Rev Microbiol, 41(1): 465–505

[120] Kishi K, Kusters-van Someren M, Mayfield M B, Sun J, Loehr T M, Gold M H (1996). Characterization of manganese(II) binding site mutants of manganese peroxidase. Biochemistry, 35(27): 8986–8994

[121] Kishi K, Wariishi H, Marquez L, Dunford H B, Gold M H (1994). Mechanism of manganese peroxidase compound II reduction. Effect of organic acid chelators and pH. Biochemistry, 33(29): 8694–8701

[122] Kleinert M, Barth T (2008). Phenols from Lignin. Chem Eng Technol, 31(5): 736–745

[123] Koenig A B, Sleighter R L, Salmon E, Hatcher P G (2010). NMR structural characterization of Quercus alba (White Oak) degraded by the brown rot fungus, Laetiporus sulphureus. J Wood Chem Technol, 30(1): 61–85

[124] Kolpak F J, Blackwell J (1976). Determination of the structure of cellulose II. Macromolecules, 9(2): 273–278

[125] Kramer K J, Kanost M R, Hopkins T L, Jiang H, Zhu Y C, Xu R, Kerwin J L, Turecek F (2001). Oxidative conjugation of catechols with proteins in insect skeletal systems. Tetrahedron, 57(2): 385–392

[126] Kuan I C, Johnson K A, Tien M (1993). Kinetic analysis of manganese peroxidase. The reaction with manganese complexes. J Biol Chem, 268(27): 20064–20070

[127] Kunamneni A, Camarero S, García-Burgos C, Plou F J, Ballesteros A, Alcalde M (2008). Engineering and applications of fungal laccases for organic synthesis. Microb Cell Fact, 7(1): 32

[128] Kuwahara M, Glenn J K, Morgan M A, Gold M H (1984). Separation and characterization of two extracelluar H₂O₂-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett, 169(2): 247–250

[129] Levasseur A, Lomascolo A, Chabrol O, Ruiz-Dueñas F J, Boukhris-Uzan E, Piumi F, Kües U, Ram A F, Murat C, Haon M, Benoit I, Arfi Y, Chevret D, Drula E, Kwon M J, Gouret P, Lesage-Meessen L, Lombard V, Mariette J, Noirot C, Park J, Patyshakuliyeva A, Sigoillot J C, Wiebenga A, Wösten H A, Martin F, Coutinho P M, de Vries R P, Martinez A T, 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, 15(1): 486

[130] Levin L, Forchiassin F, Ramos A M (2002). Copper induction of lignin-modifying enzymes in the white-rot fungus Trametes trogii. Mycologia, 94(3): 377–383

[131] Li D, Alic M, Brown J A, Gold M H (1995). Regulation of manganese peroxidase gene transcription by hydrogen peroxide, chemical stress, and molecular oxygen. Appl Environ Microbiol, 61(1): 341–345

[132] Li D, Li N, Ma B, Mayfield M B, Gold M H (1999). Characterization of genes encoding two manganese peroxidases from the lignin-degrading fungus Dichomitus squalens(1). Biochim Biophys Acta, 1434(2): 356–364

[133] Lieth H (1975) Primary Production of the Major Vegetation Units of the World. In: Lieth H, Whittaker R (eds.). Primary Productivity of the Biosphere (Ecological Studies), Springer Berlin Heidelberg, 203–215

[134] Liu S, Lu H, Hu R, Shupe A, Lin L, Liang B (2012). A sustainable woody biomass biorefinery. Biotechnol Adv, 30(4): 785–810

[135] Liu X, Du Q, Wang Z, Zhu D, Huang Y, Li N, Wei T, Xu S, Gu L (2011). Crystal structure and biochemical features of EfeB/YcdB from Escherichia coli O157: ASP235 plays divergent roles in different enzyme-catalyzed processes. J Biol Chem, 286(17): 14922–14931

[136] Lobos S, Larraín J, Salas L, Cullen D, Vicuña R (1994). Isoenzymes of manganese-dependent peroxidase and laccase produced by the lignin-degrading basidiomycete Ceriporiopsis subvermispora. Microbiology, 140(Pt 10): 2691–2698

[137] Lundell T K, Mäkelä M R, Hildén K (2010). Lignin-modifying enzymes in filamentous basidiomycetes—ecological, functional and phylogenetic review. J Basic Microbiol, 50(1): 5–20

[138] Lynd L R, Weimer P J, van Zyl W H, Pretorius I S (2002). Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev, 66(3): 506–577

[139] Ma B, Mayfield M B, Godfrey B J, Gold M H (2004). Novel promoter sequence required for manganese regulation of manganese peroxidase isozyme 1 gene expression in Phanerochaete chrysosporium. Eukaryot Cell, 3(3): 579–588

[140] Ma B, Mayfield M B, Gold M H (2001). The green fluorescent protein gene functions as a reporter of gene expression in Phanerochaete chrysosporium. Appl Environ Microbiol, 67(2): 948–955

[141] Malkin R, Malmström B G (1970). The state and function of copper in biological systems. Adv Enzymol Relat Areas Mol Biol, 33: 177–244

[142] Mancilla R A, Canessa P, Manubens A, Vicuña R (2010). Effect of manganese on the secretion of manganese-peroxidase by the basidiomycete Ceriporiopsis subvermispora. Fungal Genet Biol, 47(7): 656–661

[143] Mansur M, Suárez T, González A E (1998). Differential gene expression in the laccase gene family from basidiomycete I-62 (CECT 20197). Appl Environ Microbiol, 64(2): 771–774

[144] Manubens A, Avila M, Canessa P, Vicuña R (2003). Differential regulation of genes encoding manganese peroxidase (MnP) in the basidiomycete Ceriporiopsis subvermispora. Curr Genet, 43(6): 433–438

[145] Manubens A, Canessa P, Folch C, Avila M, Salas L, Vicuña R (2007). Manganese affects the production of laccase in the basidiomycete Ceriporiopsis subvermispora. FEMS Microbiol Lett, 275(1): 139–145

[146] Martínez A T (2002). Molecular biology and structure-function of lignin-degrading heme peroxidases. Enzyme Microb Technol, 30(4): 425–444

[147] Martínez A T, Rencoret J, Nieto L, Jiménez-Barbero J, Gutiérrez A, del Río J C (2011). Selective lignin and polysaccharide removal in natural fungal decay of wood as evidenced by in situ structural analyses. Environ Microbiol, 13(1): 96–107

[148] Martínez A T, Speranza M, Ruiz-Dueñas F J, Ferreira P, Camarero S, Guillén F, Martínez M J, Gutiérrez A, del Río J C (2005). Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol, 8(3): 195–204

[149] Martinez D, Larrondo L F, Putnam N, Gelpke M D, Huang K, Chapman J, Helfenbein K G, Ramaiya P, Detter J C, Larimer F, Coutinho P M, Henrissat B, Berka R, Cullen D, Rokhsar D (2004). Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol, 22(6): 695–700

[150] Martinez M J, Ruiz-Dueñas F J, Guillén F, Martínez A T (1996). Purification and catalytic properties of two manganese peroxidase isoenzymes from Pleurotus eryngii. Eur J Biochem, 237(2): 424–432

[151] Masai E, Katayama Y, Fukuda M (2007). Genetic and biochemical investigations on bacterial catabolic pathways for lignin-derived aromatic compounds. Biosci Biotechnol Biochem, 71(1): 1–15

[152] Mayer A M, Staples R C (2002). Laccase: new functions for an old enzyme. Phytochemistry, 60(6): 551–565

[153] Menon V, Rao M (2012). Trends in bioconversion of lignocellulose: Biofuels, platform chemicals & biorefinery concept. Prog Energ Combust, 38(4): 522–550

[154] Mester T, de Jong E, Field J A (1995). Manganese regulation of veratryl alcohol in white rot fungi and its indirect effect on lignin peroxidase. Appl Environ Microbiol, 61(5): 1881–1887

[155] Mester T, Field J A (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(25): 15412–15417

[156] Miyazaki K (2005). A hyperthermophilic laccase from Thermus thermophilus HB27. Extremophiles, 9(6): 415–425

[157] Morales M, Mate M J, Romero A, Martinez M J, Martínez A T, Ruiz-Dueñas F J (2012). Two oxidation sites for low redox potential substrates: a directed mutagenesis, kinetic, and crystallographic study on Pleurotus eryngii versatile peroxidase. J Biol Chem, 287(49): 41053–41067

[158] Moreira P R, Duez C, Dehareng D, Antunes A, Almeida-Vara E, Frère J M, Malcata F X, Duarte J C (2005). Molecular characterisation of a versatile peroxidase from a Bjerkandera strain. J Biotechnol, 118(4): 339–352

[159] Morozova O V, Shumakovich G P, Gorbacheva M A, Shleev S V, Yaropolov A I (2007). “Blue” laccases. Biochemistry (Mosc), 72(10): 1136–1150

[160] Mouso N, Papinutti L, Forchiassin F (2003). Combined effect of copper and initial pH of the culture on production of laccase and manganese peroxidase by Stereum hirsutum (Willd) Pers. Rev Iberoam Micol, 20(4): 176–178

[161] Octave S, Thomas D (2009). Biorefinery: Toward an industrial metabolism. Biochimie, 91(6): 659–664

[162] Ogola H J, 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(23): 7509–7518

[163] Ohara H (2003). Biorefinery. Appl Microbiol Biotechnol, 62(5–6): 474–477

[164] Osma J F, Toca-Herrera J L, Rodríguez-Couto S (2010). Uses of laccases in the food industry. Enzyme Res, 2010: 918761

[165] Otjen L, Blanchette R, Effland M, Leatham G (1987). Assessment of 30 White Rot Basidiomycetes for Selective Lignin Degradation Holzforschung- International Journal of the Biology, Chemistry, Physics and Technology of Wood, pp. 343

[166] Paliwal R, Rawat A P, Rawat M, Rai J P (2012). Bioligninolysis: recent updates for biotechnological solution. Appl Biochem Biotechnol, 167(7): 1865–1889

[167] Palmieri G, Giardina P, Bianco C, Fontanella B, Sannia G (2000). Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl Environ Microbiol, 66(3): 920–924

[168] Paszczynski A, Huynh V B, Crawford R (1985). Enzymatic activities of an extracellular, manganese-dependent peroxidase from Phanerochaete chrysosporium. FEMS Microbiol Lett, 29: 37–41

[169] Pauly M, Gille S, Liu L, Mansoori N, de Souza A, Schultink A, Xiong G (2013). Hemicellulose biosynthesis. Planta, 238(4): 627–642

[170] Pauly M, Keegstra K (2008). Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J, 54(4): 559–568

[171] Pérez J, Muñoz-Dorado J, de la Rubia T, Martínez J (2002). Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int Microbiol, 5(2): 53–63

[172] Pérez-Boada M, Ruiz-Dueñas F J, Pogni R, Basosi R, Choinowski T, Martínez M J, Piontek K, Martínez A T (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(2): 385–402

[173] Périé F H, Gold M H (1991). Manganese regulation of manganese peroxidase expression and lignin degradation by the white rot fungus Dichomitus squalens. Appl Environ Microbiol, 57(8): 2240–2245

[174] Peterson T W a G (2004). Top value added chemicals from biomass. no DOE/GO-102004–1992, US Department of Energy, Office of Scientific and Technical Information, Piontek K, Antorini M, Choinowski T (2002). Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-A resolution containing a full complement of coppers. J Biol Chem, 277: 37663–37669

[175] Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Faraco V (2011). Induction and transcriptional regulation of laccases in fungi. Curr Genomics, 12(2): 104–112

[176] Pogni R, Baratto M C, Teutloff C, Giansanti S, Ruiz-Dueñas F J, Choinowski T, Piontek K, Martínez A T, Lendzian F, Basosi R (2006). A tryptophan neutral radical in the oxidized state of versatile peroxidase from Pleurotus eryngii: a combined multifrequency EPR and density functional theory study. J Biol Chem, 281(14): 9517–9526

[177] Poulos T L, Edwards S L, Wariishi H, Gold M H (1993). Crystallographic refinement of lignin peroxidase at 2 A. J Biol Chem, 268(6): 4429–4440

[178] Pozdnyakova N, Makarov O, Chernyshova M, Turkovskaya O, Jarosz-Wilkolazka A (2013). Versatile peroxidase of Bjerkandera fumosa: substrate and inhibitor specificity. Enzyme Microb Technol, 52(1): 44–53

[179] Ragauskas A J, Beckham G T, Biddy M J, Chandra R, Chen F, Davis M F, Davison B H, Dixon R A, Gilna P, Keller M, Langan P, Naskar A K, Saddler J N, Tschaplinski T J, Tuskan G A, Wyman C E (2014). Lignin valorization: improving lignin processing in the biorefinery. Science, 344(6185): 1246843

[180] Ragauskas A J, Williams C K, Davison B H, Britovsek G, Cairney J, Eckert C A, Frederick W J Jr, Hallett J P, Leak D J, Liotta C L, Mielenz J R, Murphy R, Templer R, Tschaplinski T (2006). The path forward for biofuels and biomaterials. Science, 311(5760): 484–489

[181] Raj A, Reddy M M K, Chandra R (2007). Decolourisation and treatment of pulp and paper mill effluent by lignin-degrading Bacillus sp.. J Chem Tech Biot, 82(4): 399–406

[182] Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz P, Marita J, Hatfield R, Ralph S, Christensen J, Boerjan W (2004). Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl-propanoids. Phytochem Rev, 3(1/2): 29–60

[183] Ramachandra M, Crawford D L, Hertel G (1988). Characterization of an extracellular lignin peroxidase of the lignocellulolytic actinomycete Streptomyces viridosporus. Appl Environ Microbiol, 54(12): 3057–3063

[184] Ramírez D A, Muñoz S V, Atehortua L, Michel F C Jr (2010). Effects of different wavelengths of light on lignin peroxidase production by the white-rot fungi Phanerochaete chrysosporium grown in submerged cultures. Bioresour Technol, 101(23): 9213–9220

[185] Reddy G V B, Sridhar M, Gold M H (2003). Cleavage of nonphenolic β-1 diarylpropane lignin model dimers by manganese peroxidase from Phanerochaete chrysosporium. Eur J Biochem, 270(2): 284–292

[186] Reiser J, Walther I S, Fraefel C, Fiechter A (1993). Methods to investigate the expression of lignin peroxidase genes by the white rot fungus Phanerochaete chrysosporium. Appl Environ Microbiol, 59(9): 2897–2903

[187] Rico A, Rencoret J, Del Río J C, Martínez A T, Gutiérrez A (2014). Pretreatment with laccase and a phenolic mediator degrades lignin and enhances saccharification of Eucalyptus feedstock. Biotechnol Biofuels, 7(1): 6

[188] Riley R, Salamov A A, Brown D W, Nagy L G, Floudas D, Held B W, Levasseur A, Lombard V, Morin E, Otillar R, Lindquist E A, Sun H, LaButti K M, Schmutz J, Jabbour D, Luo H, Baker S E, Pisabarro A G, Walton J D, Blanchette R A, Henrissat B, Martin F, Cullen D, Hibbett D S, Grigoriev I V (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(27): 9923–9928

[189] Roberts J N, Singh R, Grigg J C, Murphy M E, Bugg T D, Eltis L D (2011). Characterization of dye-decolorizing peroxidases from Rhodococcus jostii RHA1. Biochemistry, 50(23): 5108–5119

[190] Roddy D J (2013). Biomass in a petrochemical world. Interface Focus, 3(1): 20120038

[191] Rodríguez Couto S, Toca Herrera J L (2006). Industrial and biotechnological applications of laccases: a review. Biotechnol Adv, 24(5): 500–513

[192] Ruiz-Dueñas F J, Camarero S, Pérez-Boada M, Martínez M J, Martínez A T (2001). A new versatile peroxidase from Pleurotus. Biochem Soc Trans, 29(Pt 2): 116–122

[193] Ruiz-Dueñas F J, Guillén F, Camarero S, Pérez-Boada M, Martínez M J, Martínez A T (1999). Regulation of peroxidase transcript levels in liquid cultures of the ligninolytic fungus Pleurotus eryngii. Appl Environ Microbiol, 65(10): 4458–4463

[194] Ruiz-Dueñas F J, Martínez A T (2009). Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb Biotechnol, 2(2): 164–177

[195] Ruiz-Dueñas F J, Martínez M J, Martínez A T (1999). Molecular characterization of a novel peroxidase isolated from the ligninolytic fungus Pleurotus eryngii. Mol Microbiol, 31(1): 223–235

[196] Ruiz-Dueñas F J, Morales M, García E, Miki Y, Martínez M J, Martínez A T (2009a). Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J Exp Bot, 60(2): 441–452

[197] Ruiz-Dueñas F J, Morales M, Pérez-Boada M, Choinowski T, Martínez M J, Piontek K, Martínez A T (2007). Manganese oxidation site in Pleurotus eryngii versatile peroxidase: a site-directed mutagenesis, kinetic, and crystallographic study. Biochemistry, 46(1): 66–77

[198] Ruiz-Dueñas F J, Pogni R, Morales M, Giansanti S, Mate M J, Romero A, Martínez M J, Basosi R, Martínez A T (2009b). Protein radicals in fungal versatile peroxidase: catalytic tryptophan radical in both compound I and compound II and studies on W164Y, W164H, and W164S variants. J Biol Chem, 284(12): 7986–7994

[199] Saha B C (2003). Hemicellulose bioconversion. J Ind Microbiol Biotechnol, 30(5): 279–291

[200] Salame T M, Knop D, Levinson D, Mabjeesh S J, Yarden O, Hadar Y (2012a). Release of Pleurotus ostreatus versatile-peroxidase from Mn²⁺ repression enhances anthropogenic and natural substrate degradation. PLoS One, 7(12): e52446

[201] Salame T M, Knop D, Tal D, Levinson D, Yarden O, Hadar Y (2012b). 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(15): 5341–5352

[202] Salvachúa D, Prieto A, Martínez A T, Martínez M J (2013). Characterization of a novel dye-decolorizing peroxidase (DyP)-type enzyme from Irpex lacteus and its application in enzymatic hydrolysis of wheat straw. Appl Environ Microbiol, 79(14): 4316–4324

[203] Santhanam N, Vivanco J M, Decker S R, Reardon K F (2011). Expression of industrially relevant laccases: prokaryotic style. Trends Biotechnol, 29(10): 480–489

[204] Schwarze F W M R, Engels J, Mattheck C (2000) Fungal strategies of wood decay in trees, New York, Berlin, Springer

[205] Sharma P, Goel R, Capalash N (2007). Bacterial laccases. World J Microbiol Biotechnol, 23(6): 823–832

[206] Shraddha S R, Shekher R, Sehgal S, Kamthania M, Kumar A (2011). Laccase: microbial sources, production, purification, and potential biotechnological applications. Enzyme Res, 2011: 217861

[207] Singh D, Chen S (2008). The white-rot fungus Phanerochaete chrysosporium: conditions for the production of lignin-degrading enzymes. Appl Microbiol Biotechnol, 81(3): 399–417

[208] Singh R, Grigg J C, Armstrong Z, Murphy M E, Eltis L D (2012). Distal heme pocket residues of B-type dye-decolorizing peroxidase: arginine but not aspartate is essential for peroxidase activity. J Biol Chem, 287(13): 10623–10630

[209] Soden D M, Dobson A D (2001). Differential regulation of laccase gene expression in Pleurotus sajor-caju. Microbiology, 147(Pt 7): 1755–1763

[210] Soden D M, Dobson A D (2003). The use of amplified flanking region-PCR in the isolation of laccase promoter sequences from the edible fungus Pleurotus sajor-caju. J Appl Microbiol, 95(3): 553–562

[211] Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004). Toward a systems approach to understanding plant cell walls. Science, 306(5705): 2206–2211

[212] Stewart P, Cullen D (1999). Organization and differential regulation of a cluster of lignin peroxidase genes of Phanerochaete chrysosporium. J Bacteriol, 181(11): 3427–3432

[213] Stewart P, Kersten P, Vanden Wymelenberg A, Gaskell J, Cullen D (1992). Lignin peroxidase gene family of Phanerochaete chrysosporium: complex regulation by carbon and nitrogen limitation and identification of a second dimorphic chromosome. J Bacteriol, 174(15): 5036–5042

[214] Stoj C, Kosman D J (2003). Cuprous oxidase activity of yeast Fet3p and human ceruloplasmin: implication for function. FEBS Lett, 554(3): 422–426

[215] Strittmatter E, Wachter S, Liers C, Ullrich R, Hofrichter M, Plattner D A, Piontek K (2013). Radical formation on a conserved tyrosine residue is crucial for DyP activity. Arch Biochem Biophys, 537(2): 161–167

[216] Sugano Y (2009). DyP-type peroxidases comprise a novel heme peroxidase family. Cell Mol Life Sci, 66(8): 1387–1403

[217] 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(50): 36652–36658

[218] Sundaramoorthy M, Gold M H, Poulos T L (2010). Ultrahigh (0.93A) resolution structure of manganese peroxidase from Phanerochaete chrysosporium: implications for the catalytic mechanism. J Inorg Biochem, 104(6): 683–690

[219] Sundaramoorthy M, Kishi K, Gold M H, Poulos T L (1994). The crystal structure of manganese peroxidase from Phanerochaete chrysosporium at 2.06-A resolution. J Biol Chem, 269(52): 32759–32767

[220] Sundaramoorthy M, Kishi K, Gold M H, Poulos T L (1997). Crystal structures of substrate binding site mutants of manganese peroxidase. J Biol Chem, 272(28): 17574–17580

[221] Taylor C R, Hardiman E M, Ahmad M, Sainsbury P D, Norris P R, Bugg T D (2012). Isolation of bacterial strains able to metabolize lignin from screening of environmental samples. J Appl Microbiol, 113(3): 521–530

[222] Tello M, Corsini G, Larrondo L F, Salas L, Lobos S, Vicuña R (2000). Characterization of three new manganese peroxidase genes from the ligninolytic basidiomycete Ceriporiopsis subvermispora. Biochim Biophys Acta, 1490(1–2): 137–144

[223] Thiele D J (1988). ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. Mol Cell Biol, 8(7): 2745–2752

[224] Tien M, Kirk T K (1983). Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium Burds. Science, 221(4611): 661–663

[225] Tien M, Kirk T K (1988) Lignin peroxidase of Phanerochaete chrysosporium. In: Willis A. Wood S T K (ed.). Methods in Enzymology, Academic Press, 238–249

[226] Tuck C O, Pérez E, Horváth I T, Sheldon R A, Poliakoff M (2012). Valorization of biomass: deriving more value from waste. Science, 337(6095): 695–699

[227] Valli K, Wariishi H, Gold M H (1990). Oxidation of monomethoxylated aromatic compounds by lignin peroxidase: role of veratryl alcohol in lignin biodegradation. Biochemistry, 29(37): 8535–8539

[228] Vanden Wymelenberg A, Gaskell J, Mozuch M, Kersten P, Sabat G, Martinez D, Cullen D (2009). Transcriptome and secretome analyses of Phanerochaete chrysosporium reveal complex patterns of gene expression. Appl Environ Microbiol, 75(12): 4058–4068

[229] Vanden Wymelenberg A, Gaskell J, Mozuch M, Sabat G, Ralph J, Skyba O, Mansfield S D, Blanchette R A, Martinez D, Grigoriev I, Kersten P J, Cullen D (2010). Comparative transcriptome and secretome analysis of wood decay fungi Postia placenta and Phanerochaete chrysosporium. Appl Environ Microbiol, 76(11): 3599–3610

[230] Wan C, Li Y (2012). Fungal pretreatment of lignocellulosic biomass. Biotechnol Adv, 30(6): 1447–1457

[231] Wariishi H, Akileswaran L, Gold M H (1988). Manganese peroxidase from the basidiomycete Phanerochaete chrysosporium: spectral characterization of the oxidized states and the catalytic cycle. Biochemistry, 27(14): 5365–5370

[232] Wariishi H, Gold M H (1990). Lignin peroxidase compound III. Mechanism of formation and decomposition. J Biol Chem, 265(4): 2070–2077

[233] Wariishi H, Valli K, Renganathan V, Gold M H (1989). Thiol-mediated oxidation of nonphenolic lignin model compounds by manganese peroxidase of Phanerochaete chrysosporium. J Biol Chem, 264(24): 14185–14191

[234] Welinder K G, Mauro J M, Nørskov-Lauritsen L (1992). Structure of plant and fungal peroxidases. Biochem Soc Trans, 20(2): 337–340

[235] Wesenberg D, Kyriakides I, Agathos S N (2003). White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Adv, 22(1-2): 161–187

[236] Whitwam R E, Brown K R, Musick M, Natan M J, Tien M (1997). Mutagenesis of the Mn²⁺-binding site of manganese peroxidase affects oxidation of Mn²⁺ by both compound I and compound II. Biochemistry, 36(32): 9766–9773

[237] Williamson P R, Wakamatsu K, Ito S (1998). Melanin biosynthesis in Cryptococcus neoformans. J Bacteriol, 180(6): 1570–1572

[238] Wong D W (2009). Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotechnol, 157(2): 174–209

[239] Xiao X, Marzluf G A (1996). Identification of the native NIT2 major nitrogen regulatory protein in nuclear extracts of Neurospora crassa. Genetica, 97(2): 153–163

[240] Xiao Y Z, Hong Y Z, Li J F, Hang J, Tong P G, Fang W, Zhou C Z (2006). Cloning of novel laccase isozyme genes from Trametes sp. AH28-2 and analyses of their differential expression. Appl Microbiol Biotechnol, 71(4): 493–501

[241b] Xu F, Shin W, Brown S H, Wahleithner J A, Sundaram U M, Solomon E I (1996). A study of a series of recombinant fungal laccases and bilirubin oxidase that exhibit significant differences in redox potential, substrate specificity, and stability. BiochimBiophysActa, 1292: 303–311

[241] Yaropolov A I, Skorobogat’ko O V, Vartanov S S, Varfolomeyev S D (1994). Laccase. Appl Biochem Biotechnol, 49(3): 257–280

[242] Yelle D J, Ralph J, Lu F, Hammel K E (2008). Evidence for cleavage of lignin by a brown rot basidiomycete. Environ Microbiol, 10(7): 1844–1849

[243] Yoshida H, the Communication from the Chemical Society of Tokio (1883). Yoshida: Chemistry of lacquer (Urushi). J Chem Soc Trans, 43: 472–486

[244] Yoshida T, Tsuge H, Konno H, Hisabori T, Sugano Y (2011). The catalytic mechanism of dye-decolorizing peroxidase DyP may require the swinging movement of an aspartic acid residue. FEBS J, 278(13): 2387–2394

[245] Zeng Y, Zhao S, Yang S, Ding S Y (2014). Lignin plays a negative role in the biochemical process for producing lignocellulosic biofuels. Curr Opin Biotechnol, 27: 38–45

[246] Zhang Y H (2008). Reviving the carbohydrate economy via multi-product lignocellulose biorefineries. J Ind Microbiol Biotechnol, 35(5): 367–375

[247] Zimmermann W (1990). Degradation of lignin by bacteria. J Biotechnol, 13(2–3): 119–130

[248] Zubieta C, Joseph R, Krishna S S, McMullan D, Kapoor M, Axelrod H L, Miller M D, Abdubek P, Acosta C, Astakhova T, Carlton D, Chiu H J, Clayton T, Deller M C, Duan L, Elias Y, Elsliger M A, Feuerhelm J, Grzechnik S K, Hale J, Han G W, Jaroszewski L, Jin K K, Klock H E, Knuth M W, Kozbial P, Kumar A, Marciano D, Morse A T, Murphy K D, Nigoghossian E, Okach L, Oommachen S, Reyes R, Rife C L, Schimmel P, Trout C V, van den Bedem H, Weekes D, White A, Xu Q, Hodgson K O, Wooley J, Deacon A M, Godzik A, Lesley S A, Wilson I A (2007). Identification and structural characterization of heme binding in a novel dye-decolorizing peroxidase, TyrA. Proteins: Struct, Funct. Bioinf, 69: 234–243

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg