DyP-like peroxidases of the jelly fungus Auricularia auricula-judae oxidize nonphenolic lignin model compounds and high-redox potential dyes

Applied Microbiology and Biotechnology

Volumn 85, Issue 6, 2010, Pages 1869-1879

  Liers, Christiane ^a   Bobeth, Caroline ^a   Pecyna, Marek ^a   Ullrich, René ^a   Hofrichter, Martin ^a  

^a International Graduate School Zittau   (Germany)

Author keywords

Azo and anthraquinone dyes; Dye decolorizing peroxidases; Jelly fungi; Nonphenolic O 4 lignin model compound; White rot

Indexed keywords

AGITATED CULTURE; ANTHRAQUINONE DYE; AURICULARIA AURICULA; AZO AND ANTHRAQUINONE DYES; BEECH WOOD; ELECTROPHORETIC ANALYSIS; ENZYMATIC ACTIVITIES; FUNGAL ENZYMES; LIGNIN MODEL COMPOUND; LIGNIN MODELS; N-TERMINAL AMINO ACID SEQUENCE; NON-PHENOLIC LIGNIN; PEROXIDASE ACTIVITIES; PURIFIED PROTEIN; REACTIVE BLACK 5; REACTIVE BLUE 5; REDOX POTENTIALS; VERATRYL ALCOHOL; WHITE ROT;

AMINO ACIDS; ENZYMES; FUNGI; KETONES; LIGNIN; MANGANESE; MANGANESE COMPOUNDS; ORGANIC ACIDS; PORPHYRINS; SECONDARY BATTERIES;

DYES;

ADLEROL; ALCOHOL DERIVATIVE; AURICULARIA AURICULA JUDAE PEROXIDASE I; AURICULARIA AURICULA JUDAE PEROXIDASE II; DYE; FUNGAL ENZYME; REACTIVE BLACK 5; REACTIVE BLUE 5; UNCLASSIFIED DRUG; VERATRYL ALCOHOL;

AMINO ACID; DYE; ENZYME ACTIVITY; FUNGUS; LIGNIN; PH; PROTEIN; WOOD;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; AURICULARIA AURICULA JUDAE; CONTROLLED STUDY; DECOLORIZATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME METABOLISM; ENZYME PURIFICATION; ENZYME SUBSTRATE; ENZYME SYNTHESIS; FUNGUS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; NONHUMAN; SEQUENCE HOMOLOGY;

BASIDIOMYCOTA; COLORING AGENTS; FUNGAL PROTEINS; LIGNIN; MODELS, CHEMICAL; OXIDATION-REDUCTION; PEROXIDASE; SEQUENCE HOMOLOGY, AMINO ACID;

AMINO ACIDS; BATTERIES; DYES; FUNGI; KETONES; LIGNINS; MANGANESE COMPOUNDS; ORGANIC ACIDS; PEROXIDASE;

AURICULARIA AURICULA-JUDAE; FAGUS; LYCOPERSICON ESCULENTUM; MARASMIUS SCORODONIUS; TERMITOMYCES ALBUMINOSUS; THANATEPHORUS CUCUMERIS; TREMELLALES;

EID: 76849083614     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-009-2173-7     Document Type: Article

References (59)

1. E Adler 1977 Lignin chemistry-past, present and future Wood Sci Technol 11 169 218 10.1007/BF00365615 1:CAS:528:DyaE1cXisVeruw%3D%3D
2. MD Aitken RL Irvine 1989 Stability testing of ligninase and Mn-peroxidase from Phanerochaete chrysosporium Biotechnol Bioeng 34 1251 1260 10.1002/bit.260341003 1:CAS:528:DyaK3cXltFWnsA%3D%3D
3. DH Anh R Ullrich D Benndorf A Svatos A Muck M Hofrichter 2007 The coprophilous mushroom Coprinus radians secretes a haloperoxidase that catalyzes aromatic peroxygenation Appl Environ Microbiol 73 5477 5485 10.1128/AEM.00026-07 1:CAS:528:DC%2BD2sXhtVeht7%2FO (Pubitemid 47378751)
4. C Bohlin P Persson L Gorton K Lundquist LJ Jönsson 2005 Product profiles in enzymic and non-enzymic oxidations of the lignin model compound erythro-1-(3, 4-dimethoxyphenyl)-2-(2-methoxyphenoxy)-1, 3-propanediol J Mol Catal B: Enzym 35 100 107 10.1016/j.molcatb.2005.06.003 1:CAS:528: DC%2BD2MXosVCktb4%3D (Pubitemid 41557489)
5. JM Bollag RD Sjoblad SY Liu 1979 Characterization of an enzyme from Rhizoctonia praticola which polymerizes phenolic compounds Can J Microbiol 25 229 233 1:CAS:528:DyaE1MXhsVOmsbg%3D
6. S Camarero S Sarkar FJ Ruiz-Duenas MJ Martinez AT Martinez 1999 Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites J Biol Chem 274 10324 10330 10.1074/jbc.274.15.10324 1:CAS:528:DyaK1MXis1GjtbY%3D (Pubitemid 29180907)
7. L Caramelo MJ Martinez AT Martinez 1999 A search for ligninolytic peroxidases in the fungus Pleurotus eryngii involving α-keto-γ- thiomethylbutyric acid and lignin model dimers Appl Environ Microbiol 65 916 922 1:CAS:528:DyaK1MXhslWktro%3D
8. N Chung SD Aust 1995 Inactivation of lignin peroxidase by hydrogen peroxide during the oxidation of phenols Arch Biochem Biophys 316 851 855 10.1006/abbi.1995.1114 1:CAS:528:DyaK2MXjs1Ojsr4%3D
9. Cullen D, Kersten PJ (2004) Enzymology and molecular biology of lignin degradation. In: Brambl R, Marzluf GA (eds) The Mycota, vol 3. Biochemistry and molecular biology, 2nd edn. Springer, Berlin, pp 249-273
10. C Eggert U Temp JF Dean KE Eriksson 1996 A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase FEBS Lett 391 144 148 10.1016/0014-5793(96)00719-3 1:CAS:528:DyaK28XkvFWitLw%3D (Pubitemid 26325732)
11. V Faraco A Piscitelli G Sannia P Giardina 2007 Identification of a new member of the dye-decolorizing peroxidase family from Pleurotus ostreatus World J Microbiol Biotechnol 23 889 893 10.1007/s11274-006-9303-5 1:CAS:528: DC%2BD2sXltVGqu7w%3D (Pubitemid 46742104)
12. Gamauf C, Metz B, Seiboth B (2007) Degradation of plant cell wall polymers by fungi. In: Kubicek CP, Druzhinina IS (eds) The Mycota, vol 4. Environmental and microbial relationships, 2nd edn. Springer, Berlin, pp 325-339
13. IG Gazarian LM Lagrimini SJ George RN Thorneley 1996 Anionic tobacco peroxidase is active at extremely low pH: veratryl alcohol oxidation with a pH optimum of 1.8 Biochem J 320 369 372 1:CAS:528:DyaK2sXis1Gn
14. MDS Gelpke J Lee MH Gold 2002 Lignin peroxidase oxidation of veratryl alcohol: effects of the mutants H82A, Q222A, W171A, and F267L Biochemistry 41 3498 3506 10.1021/bi011930d (Pubitemid 34214047)
15. 2-requiring diarylpropane oxygenase from the white rot basidiomycete, Phanerochaete chrysosporium Arch Biochem Biophys 234 353 362 10.1016/0003-9861(84)90280-7 1:CAS:528:DyaL2MXitVWitA%3D%3D
16. Hatakka A (2001) Biodegradation of lignin. In: Hofrichter M, Steinbüchel A (eds) Biopolymers. Lignin, humic substances and coal, vol 1. Wiley-VCH, Weinheim, pp 129-180
17. A Hatakka TK Lundell ALM Tervilä-Wilo G Brunow 1991 Metabolism of non-phenolic β-O-4 lignin model compounds by the white-rot fungus Phlebia radiata Appl Microbiol Biotechnol 36 270 277 10.1007/BF00164433 1:CAS:528:DyaK38XhtVagu78%3D
18. A Heinfling MJ Martinez AT Martinez M Bergbauer U Szewzyk 1998 Purification and characterization of peroxidases from the dye-decolorizing fungus Bjerkandera adusta FEMS Microbiol Lett 165 43 50 10.1111/j.1574-6968. 1998.tb13125.x 1:CAS:528:DyaK1cXltlKrt7Y%3D
19. A Heinfling FJ Ruiz-Duenas MJ Martinez M Bergbauer U Szewzyk AT Martinez 1998 A study on reducing substrates of manganese-oxidizing peroxidases from Pleurotus eryngii and Bjerkandera adusta FEBS Lett 428 141 146 10.1016/S0014-5793(98)00512-2 1:CAS:528:DyaK1cXjt1Cmur0%3D (Pubitemid 28319673)
20. M Heinzkill L Bech T Halkier P Schneider T Anke 1998 Characterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae) Appl Environ Microbiol 64 1601 1606 1:CAS:528:DyaK1cXislWmurY%3D
21. DS Hibbett 2006 A phylogenetic overview of the Agaricomycotina Mycologia 98 917 925 10.3852/mycologia.98.6.917
22. M Hofrichter D Ziegenhagen T Vares M Friedrich MG Jager W Fritsche A Hatakka 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 10.1016/S0014-5793(98)01023-0 1:CAS:528:DyaK1cXmt1yjurg%3D (Pubitemid 29052257)
23. M Hofrichter T Lundell A Hatakka 2001 Conversion of milled pine wood by manganese peroxidase from Phlebia radiata Appl Environ Microbiol 67 4588 4593 10.1128/AEM.67.10.4588-4593.2001 1:CAS:528:DC%2BD3MXns1Wisb4%3D (Pubitemid 33646088)
24. DM Hushpulian AA Poloznikov PA Savitski AM Rozhkova TA Chubar VA Fechina MA Orlova VI Tishkov IG Gazaryan LM Lagrimini 2007 Glutamic acid-141: a heme 'bodyguard' in anionic tobacco peroxidase Biol Chem 388 373 380 10.1515/BC.2007.050 1:CAS:528:DC%2BD2sXjvVymtLc%3D (Pubitemid 46514694)
25. SJ Kim M Shoda 1999 Purification and characterization of a novel peroxidase from Geotrichum candidum Dec 1 involved in decolorization of dyes Appl Environ Microbiol 65 1029 1035 1:CAS:528:DyaK1MXhslWktL8%3D
26. TK Kirk E Schulz WJ Connors LF Lorenz JG Zeikus 1978 Influence of culture parameters on lignin metabolism by Phanerochaete chrysosporium Arch Microbiol 177 277 285 10.1007/BF00738547
27. TK Kirk M Tien PJ Kersten MD Mozuch B Kalyanaraman 1986 Ligninase of Phanerochaete chrysosporium. Mechanism of its degradation of the non-phenolic arylglycerol-β-aryl ether substructure of lignin Biochem J 236 279 287 1:CAS:528:DyaL28Xkt1SqsLc%3D
28. UK Laemmli 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680 685 10.1038/227680a0 1:CAS:528:DC%2BD3MXlsFags7s%3D
29. 14C-labelled synthetic lignin and extracellular enzyme activities of the wood-colonizing ascomycetes Xylaria hypoxylon and Xylaria polymorpha Appl Microbiol Biotechnol 69 573 579 10.1007/s00253-005-0010-1 1:CAS:528: DC%2BD2MXhtlemurvP (Pubitemid 41830869)
30. T Lundell A Hatakka 1994 Participation of Mn(II) in the catalysis of laccase, manganese peroxidase and lignin peroxidase from Phlebia radiata FEBS Lett 348 291 296 10.1016/0014-5793(94)00627-X 1:CAS:528:DyaK2cXmt1Crtrg%3D (Pubitemid 24223060)
31. Lundell TK, Kileläinen IA, Brunow G, Schoemaker HE, Hatakka A (1992) Degradation of macromolecular lignin models by lignin peroxidase from Phlebia radiata and catalytic properties of the enzyme. Paper presented at the 5th International Conference on Biotechnology in the Pulp and Paper Industry. Kyoto, Japan
32. T Lundell R Wever R Floris P Harvey A Hatakka G Brunow H Schoemaker 1993 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 10.1111/j.1432-1033.1993.tb17562.x 1:CAS:528:DyaK3sXhvVKltLs%3D (Pubitemid 23050006)
33. MJ Martinez FJ Ruiz-Duenas F Guillen AT Martinez 1996 Purification and catalytic properties of two manganese peroxidase isoenzymes from Pleurotus eryngii Eur J Biochem 237 424 432 10.1111/j.1432-1033.1996.0424k.x 1:CAS:528:DyaK28XisFWjt7g%3D
34. JP McEldoon AR Pokora JS Dordick 1995 Lignin peroxidase-type activity of soybean peroxidase Enzyme Microb Technol 17 359 365 10.1016/0141-0229(94)00060-3 1:CAS:528:DyaK2MXlsVeisL4%3D (Pubitemid 26032784)
35. T Mester JA Field 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 10.1074/jbc.273.25.15412 1:CAS:528:DyaK1cXktVSmt7s%3D (Pubitemid 28298146)
36. I Morgenstern S Klopman DS Hibbett 2008 Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes J Mol Evol 66 243 257 10.1007/s00239-008-9079-3 1:CAS:528:DC%2BD1cXlsV2nu7w%3D
37. M Pecyna R Ullrich B Bittner A Clemens R Schubert K Scheibner M Hofrichter 2009 Molecular characterization of aromatic peroxygenase from Agrocybe aegerita Appl Microbiol Biotechnol 10.1007/s00253-009-2000-1:
38. TL Poulos SL Edwards H Wariishi MH Gold 1993 Crystallographic refinement of lignin peroxidase at 2 A J Biol Chem 268 4429 4440 1:CAS:528: DyaK3sXitVynsb4%3D
39. I Robene-Soustrade B Lung-Escarmant JJ Bono B Taris 1992 Identification and partial characterization of an extracellular manganese-dependent peroxidase in Armillaria ostoyae and Armillaria mellea Eur J For Pathol 22 227 236 10.1111/j.1439-0329.1992.tb00787.x
40. M Scheibner B Hulsdau K Zelena M Nimtz L de Boer RG Berger H Zorn 2008 Novel peroxidases of Marasmius scorodonius degrade β-carotene Appl Microbiol Biotechnol 77 1241 1250 10.1007/s00253-007-1261-9 1:CAS:528: DC%2BD1cXhsFSjtr4%3D
41. Schmidt O (2006) Wood and tree fungi. Biology, damage, protection, and use. Springer, Berlin
42. HE Schoemaker TK Lundell A Hatakka K Piontek 1994 The oxidation of veratryl alcohol, dimeric lignin models and lignin by lignin peroxidase: redox cycle revisited FEMS Microbiol Rev 13 321 332 10.1111/j.1574-6976.1994.tb00052.x 1:CAS:528:DyaK2cXislegs7s%3D (Pubitemid 124001068)
43. T Shimokawa M Hirai M Shoda Y Sugano 2008 Efficient dye decolorization and production of dye decolorizing enzymes by the basidiomycete Thanatephorus cucumeris Dec 1 in a liquid and solid hybrid culture J Biosci Bioeng 106 481 487 10.1263/jbb.106.481 1:CAS:528:DC%2BD1MXhvVyms74%3D
44. T Shimokawa M Shoda Y Sugano 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 10.1016/j.jbiosc.2008.09.013 1:CAS:528:DC%2BD1MXkvFGltrg%3D
45. Y Sugano 2009 DyP-type peroxidases comprise a novel heme peroxidase family Cell Mol Life Sci 66 1387 1403 10.1007/s00018-008-8651-8 1:CAS:528:DC%2BD1MXksFGhtb0%3D
46. Y Sugano K Sasaki M Shoda 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 10.1016/S1389-1723(99)80087-5 1:CAS:528: DyaK1MXkvFajsb0%3D (Pubitemid 29239000)
47. Y Sugano R Nakano K Sasaki M Shoda 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 10.1128/AEM.66.4.1754-1758.2000 1:CAS:528:DC%2BD3cXisVWlt78%3D (Pubitemid 30185667)
48. Y Sugano R Muramatsu A Ichiyanagi T Sato M Shoda 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 10.1074/jbc.M706996200 1:CAS:528:DC%2BD2sXhsVSgtrfI
49. Y Sugano Y Matsushima K Tsuchiya H Aoki M Hirai M Shoda 2009 Degradation pathway of an anthraquinone dye catalyzed by a unique peroxidase DyP from Thanatephorus cucumeris Dec 1 Biodegradation 20 433 440 10.1007/s10532-008-9234- y 1:CAS:528:DC%2BD1MXlsVSisbw%3D
50. R Ten Have S Hartmans PJ Teunissen JA Field 1998 Purification and characterization of two lignin peroxidase isozymes produced by Bjerkandera sp. strain BOS55 FEBS Lett 422 391 394 10.1016/S0014-5793(98)00044-1 (Pubitemid 28075502)
51. M Tien TK Kirk 1988 Lignin peroxidase of Phanerochaete chrysosporium Methods Enzymol 161 238 249 10.1016/0076-6879(88)61025-1 1:CAS:528: DyaL1MXhs1yqtbo%3D
52. H Tuisel R Sinclair JA Bumpus W Ashbaugh BJ Brock SD Aust 1990 Lignin peroxidase H2 from Phanerochaete chrysosporium: purification, characterization and stability to temperature and pH Arch Biochem Biophys 279 158 166 10.1016/0003-9861(90)90476-F 1:CAS:528:DyaK3cXktVansrs%3D (Pubitemid 20149787)
53. R Ullrich J Nuske K Scheibner J Spantzel M Hofrichter 2004 Novel haloperoxidase from the agaric basidiomycete Agrocybe aegerita oxidizes aryl alcohols and aldehydes Appl Environ Microbiol 70 4575 4581 10.1128/AEM.70.8. 4575-4581.2004 1:CAS:528:DC%2BD2cXms1eltLk%3D (Pubitemid 39095478)
54. R Ullrich C Liers S Schimpke M Hofrichter 2009 Purification of homogeneous forms of fungal peroxygenase J Biotechnol. 10.1002/biot.200900076:
55. G Ward Y Hadar I Bilkis CG Dosoretz 2003 Mechanistic features of lignin peroxidase-catalyzed oxidation of substituted phenols and 1, 2-dimethoxyarenes J Biol Chem 278 39726 39734 10.1074/jbc.M303918200 1:CAS:528:DC%2BD3sXnvFanurk%3D (Pubitemid 37248534)
56. M Wei F Oberwinkler 2001 Phylogenetic relationships in Auriculariales and related groups-hypotheses derived from nuclear ribosomal DNA sequences Mycol Res 105 403 415 10.1017/S095375620100363X (Pubitemid 32398552)
57. KG Welinder 1992 Superfamily of plant, fungal and bacterial peroxidases Curr Opin Struct Biol 2 388 393 10.1016/0959-440X(92)90230-5 1:CAS:528:DyaK38XltVKrsLY%3D
58. C Zubieta R Joseph SS Krishna D McMullan M Kapoor HL Axelrod MD Miller P Abdubek C Acosta T Astakhova D Carlton HJ Chiu T Clayton MC Deller L Duan Y Elias MA Elsliger J Feuerhelm SK Grzechnik J Hale GW Han L Jaroszewski KK Jin HE Klock MW Knuth P Kozbial A Kumar D Marciano AT Morse KD Murphy E Nigoghossian L Okach S Oommachen R Reyes CL Rife P Schimmel CV Trout H van den Bedem D Weekes A White Q Xu KO Hodgson J Wooley AM Deacon A Godzik SA Lesley IA Wilson 2007 Identification and structural characterization of heme binding in a novel dye-decolorizing peroxidase, TyrA Proteins 69 234 243 10.1002/prot.21673 1:CAS:528:DC%2BD2sXhtVykt7rI (Pubitemid 47429287)
59. C Zubieta SS Krishna M Kapoor P Kozbial D McMullan HL Axelrod MD Miller P Abdubek E Ambing T Astakhova D Carlton HJ Chiu T Clayton MC Deller L Duan MA Elsliger J Feuerhelm SK Grzechnik J Hale E Hampton GW Han L Jaroszewski KK Jin HE Klock MW Knuth A Kumar D Marciano AT Morse E Nigoghossian L Okach S Oommachen R Reyes CL Rife P Schimmel H van den Bedem D Weekes A White Q Xu KO Hodgson J Wooley AM Deacon A Godzik SA Lesley IA Wilson 2007 Crystal structures of two novel dye-decolorizing peroxidases reveal a β-barrel fold with a conserved heme-binding motif Proteins 69 223 233 10.1002/prot.21550 1:CAS:528: DC%2BD2sXhtVykt7rP (Pubitemid 47429286)