A comparative genomic analysis of the oxidative enzymes potentially involved in lignin degradation by Agaricus bisporus

Fungal Genetics and Biology

Volumn 55, Issue , 2013, Pages 22-31

  Doddapaneni, Harshavardhan ^a   Subramanian, Venkataramanan ^b,d   Fu, Bolei ^a   Cullen, Dan ^c  

^a UNIVERSITY OF IOWA   (United States)

^b Department of Geology and Geological Engineering   (United States)

^c FOREST PRODUCTS LABORATORY   (United States)

^d NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

Author keywords

Agaricus bisporus; Comparative genomics; Cytochrome P450 monooxygenase; Litter rot fungi; Oxidase; Peroxidase

Indexed keywords

COPPER RADICAL REDUCTASE; CYTOCHROME P450; LACCASE; LIGNIN; LIGNOCELLULOSE; MANGANESE PEROXIDASE; OXIDOREDUCTASE; PEROXIDASE; THIOLATE PEROXIDASE; UNCLASSIFIED DRUG;

AGARICUS BISPORUS; ARTICLE; COMPARATIVE STUDY; COPRINOPSIS CINEREA; FUNGAL GENE; FUNGUS; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; GENOMICS; LACCARIA; LACCARIA BICOLOR; NONHUMAN; NUCLEOTIDE SEQUENCE; PHANEROCHAETE; POSTIA PLACENTA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; SPECIES DIFFERENTIATION; SPECIES DIVERSITY;

AGARICUS; BIOTRANSFORMATION; COMPUTATIONAL BIOLOGY; FUNGAL PROTEINS; GENETIC VARIATION; GENOME, FUNGAL; LIGNIN; METABOLIC NETWORKS AND PATHWAYS; OXIDOREDUCTASES;

AGARICUS BISPORUS; COPRINOPSIS CINEREA; FUNGI; LACCARIA BICOLOR; PHANEROCHAETE CHRYSOSPORIUM; POSTIA PLACENTA;

EID: 84879016211     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.03.004     Document Type: Article

References (74)

1. Agger S., Lopez-Gallego F., Schmidt-Dannert C. Diversity of sesquiterpene synthases in the basidiomycete Coprinus cinereus. Mol. Microbiol. 2009, 72:1181-1195.
2. Akiyama R., Sato Y., Kajiwara S., Shishido K. Cloning and expression of cytochrome P450 genes, belonging to a new P450 family, of the basidiomycete Lentinula edodes. Biosci. Biotechnol. Biochem. 2002, 66:2183-2188.
3. Andreou A., Brodhun F., Feussner I. Biosynthesis of oxylipins in non-mammals. Prog. Lipid Res. 2009, 48:148-170.
4. Anzenbacher P., Anzenbacherova E. Cytochromes P450 and metabolism of xenobiotics. Cell. Mol. Life Sci. 2001, 58:737-747.
5. Baldrian P. Fungal laccases - occurrence and properties. FEMS Microbiol. Rev. 2006, 30:215-242.
6. Bonnen A.M., Anton L.H., Orth A.B. Lignin-degrading enzymes of the commercial button mushroom, Agaricus bisporus. Appl. Environ. Microbiol. 1994, 60:960-965.
7. Courty P.E., Hoegger P.J., Kilaru S., Kohler A., Buee M., Garbaye J., Martin F., Kues U. Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol. 2009, 182:736-750.
8. Cullen D. Recent advances on the molecular genetics of ligninolytic fungi. J. Biotechnol. 1997, 53:273-289.
9. Doddapaneni H., Chakraborty R., Yadav J.S. Genome-wide structural and evolutionary analysis of the P450 monooxygenase genes (P450ome) in the white rot fungus Phanerochaete chrysosporium: evidence for gene duplications and extensive gene clustering. BMC Genom. 2005, 6:92.
10. Durrant A.J., Wood D.A., Cain R.B. Lignocellulose biodegradation by Agaricus bisporus during solid substrate fermentation. J. Gen. Microbiol. 1991, 137:751-755.
11. Eastwood D.C., Floudas D., Binder M., Majcherczyk A., Schneider P., Aerts A., Asiegbu F.O., Baker S.E., Barry K., Bendiksby M., Blumentritt M., Coutinho P.M., Cullen D., de Vries R.P., Gathman A., Goodell B., Henrissat B., Ihrmark K., Kauserud H., Kohler A., LaButti K., Lapidus A., Lavin J.L., Lee Y.H., Lindquist E., Lilly W., Lucas S., Morin E., Murat C., Oguiza J.A., Park J., Pisabarro A.G., Riley R., Rosling A., Salamov A., Schmidt O., Schmutz J., Skrede I., Stenlid J., Wiebenga A., Xie X., Kues U., Hibbett D.S., Hoffmeister D., Hogberg N., Martin F., Grigoriev I.V., Watkinson S.C. The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 2011, 333:762-765.
12. Eriksson K.-E.L. Microbial and Enzymatic Degradation of Wood and Wood Components 1990, Springer Verlag, Berlin.
13. Fernandez-Fueyo E., Ruiz-Duenas 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., 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., Lavin 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., Kues 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. Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc. Natl. Acad. Sci. USA 2012, 109:5458-5463.
14. Floudas D., Binder M., Riley R., Barry K., Blanchette R.A., Henrissat B., Martinez 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., Gorecki P., Heitman J., Hesse C., Hori C., Igarashi K., Jurgens J.A., Kallen N., Kersten P., Kohler A., Kues 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-Duenas 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. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 2012, 336:1715-1719.
15. Fukuda H., Nakamura K., Sukita E., Ogawa T., Fujii T. Cytochrome P450rm from Rhodotorula minuta catalyzes 4-hydroxylation of benzoate. J. Biochem. 1996, 119:314-318.
16. Hammel K.E., Cullen D. Role of fungal peroxidases in biological ligninolysis. Curr. Opin. Plant Biol. 2008, 11:349-355.
17. 2 recycling during oxidation of the arylglycerol beta-aryl ether lignin structure by lignin peroxidase and glyoxal oxidase. Biochemistry 1994, 33:13349-13354.
18. Hatakka A. Lignin-modifying enzymes from selected white-rot fungi: production and role in lignin degradation. FEMS Microbiol. Rev. 1994, 13:125-135.
19. Hernandez-Ortega A., Ferreira P., Martinez A.T. Fungal aryl-alcohol oxidase: a peroxide-producing flavoenzyme involved in lignin degradation. Appl. Microbiol. Biotechnol. 2012, 93:1395-1410.
20. Hilden K., Hakala T.K., Lundell T. Thermotolerant and thermostable laccases. Biotechnol. Lett. 2009, 31:1117-1128.
21. Hirano T., Sato T., Enei H. Isolation of genes specifically expressed in the fruit body of the edible basidiomycete Lentinula edodes. Biosci. Biotechnol. Biochem. 2004, 68:468-472.
22. Hofrichter M., Ullrich R. New trends in fungal biooxidation. The Mycota 2010, 425-437. Springer-Verlag, Berlin. K. Esser (Ed.).
23. Hofrichter M., Ullrich R., Pecyna M.J., Liers C., Lundell T. New and classic families of secreted fungal heme peroxidases. Appl. Microbiol. Biotechnol. 2010, 87:871-897.
24. Hohn T.M., Desjardins A.E., McCormick S.P. The Tri4 gene of Fusarium sporotrichioides encodes a cytochrome P450 monooxygenase involved in trichothecene biosynthesis. Mol. Gen. Genet. 1995, 248:95-102.
25. Ichinose H. Molecular and functional diversity of fungal cytochrome P450s. Biol. Pharm. Bull. 2012, 35:833-837.
26. Ide M., Ichinose H., Wariishi H. Molecular identification and functional characterization of cytochrome P450 monooxygenases from the brown-rot basidiomycete Postia placenta. Arch. Microbiol. 2012, 194:243-253.
27. Kelly D.E., Krasevec N., Mullins J., Nelson D.R. The CYPome (Cytochrome P450 complement) of Aspergillus nidulans. Fungal Genet. Biol. 2009, 46(Suppl. 1):S53-61.
28. Kim S.J., Shoda M. Purification and characterization of a novel peroxidase from Geotrichum candidum dec 1 involved in decolorization of dyes. Appl. Environ. Microbiol. 1999, 65:1029-1035.
29. Kirk T.K., Farrell R.L. Enzymatic "combustion": the microbial degradation of lignin. Annu. Rev. Microbiol. 1987, 41:465-505.
30. Kullman S.W., Matsumura F. Metabolic pathways utilized by Phanerochaete chrysosporium for degradation of the cyclodiene pesticide endosulfan. Appl. Environ. Microbiol. 1996, 62:593-600.
31. Lankinen P., Hilden K., Aro N., Salkinoja-Salonen M., Hatakka A. Manganese peroxidase of Agaricus bisporus: grain bran-promoted production and gene characterization. Appl. Microbiol. Biotechnol. 2005, 66:401-407.
32. Leonowicz A., Cho N.S., Luterek J., Wilkolazka A., Wojtas-Wasilewska M., Matuszewska A., Hofrichter M., Wesenberg D., Rogalski J. Fungal laccase: properties and activity on lignin. J. Basic Microbiol. 2001, 41:185-227.
33. Lettera V., Piscitelli A., Leo G., Birolo L., Pezzella C., Sannia G. Identification of a new member of Pleurotus ostreatus laccase family from mature fruiting body. Fungal Biol. 2010, 114:724-730.
34. 2-producing glyoxal oxidase is required for filamentous growth and pathogenicity in Ustilago maydis. Mol. Genet. Genom. 2005, 272:639-650.
35. Liers C., Pecyna M.J., Kellner H., Worrich A., Zorn H., Steffen K.T., Hofrichter M., Ullrich R. Substrate oxidation by dye-decolorizing peroxidases (DyPs) from wood- and litter-degrading agaricomycetes compared to other fungal and plant heme-peroxidases. Appl. Microbiol. Biotechnol. 2012.
36. Martinez A.T. Molecular biology and structure-function of lignin-degrading heme peroxidases. Enzyme Microb. Technol. 2002, 30:425-444.
37. 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. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat. Biotechnol. 2004, 22:695-700.
38. Martinez A.T., Speranza M., Ruiz-Duenas F.J., Ferreira P., Camarero S., Guillen F., Martinez M.J., Gutierrez A., del Rio J.C. Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int. Microbiol. 2005, 8:195-204.
39. Martinez D., Challacombe J., Morgenstern I., Hibbett D., Schmoll M., Kubicek C.P., Ferreira P., Ruiz-Duenas F.J., Martinez A.T., Kersten P., Hammel K.E., Vanden Wymelenberg A., Gaskell J., Lindquist E., Sabat G., Bondurant S.S., Larrondo L.F., Canessa P., Vicuna R., Yadav J., Doddapaneni H., Subramanian V., Pisabarro A.G., Lavin J.L., Oguiza J.A., Master E., Henrissat B., Coutinho P.M., Harris P., Magnuson J.K., Baker S.E., Bruno K., Kenealy W., Hoegger P.J., Kues U., Ramaiya P., Lucas S., Salamov A., Shapiro H., Tu H., Chee C.L., Misra M., Xie G., Teter S., Yaver D., James T., Mokrejs M., Pospisek M., Grigoriev I.V., Brettin T., Rokhsar D., Berka R., Cullen D. Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc. Natl. Acad. Sci. USA 2009, 106:1954-1959.
40. Martinez A.T., Rencoret J., Nieto L., Jimenez-Barbero J., Gutierrez A., del Rio J.C. Selective lignin and polysaccharide removal in natural fungal decay of wood as evidenced by in situ structural analyses. Environ. Microbiol. 2011, 13:96-107.
41. Matsuzaki F., Wariishi H. Molecular characterization of cytochrome P450 catalyzing hydroxylation of benzoates from the white-rot fungus Phanerochaete chrysosporium. Biochem. Biophys. Res. Commun. 2005, 334:1184-1190.
42. Mayer A.M., Staples R.C. Laccase: new functions for an old enzyme. Phytochemistry 2002, 60:551-565.
43. Morin E., Kohler A., Baker A.R., Foulongne-Oriol M., Lombard V., Nagy L.G., Ohm R.A., Patyshakuliyeva A., Brun A., Aerts A.L., Bailey A.M., Billette C., Coutinho P.M., Deakin G., Doddapaneni H., Floudas D., Grimwood J., Hilden K., Kues U., Labutti K.M., Lapidus A., Lindquist E.A., Lucas S.M., Murat C., Riley R.W., Salamov A.A., Schmutz J., Subramanian V., Wosten H.A., Xu J., Eastwood D.C., Foster G.D., Sonnenberg A.S., Cullen D., de Vries R.P., Lundell T., Hibbett D.S., Henrissat B., Burton K.S., Kerrigan R.W., Challen M.P., Grigoriev I.V., Martin F. Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc. Natl. Acad. Sci. USA 2012, 109:17501-17506.
44. Morris D.R., Hager L.P. Chloroperoxidase. I. Isolation and properties of the crystalline glycoprotein. J. Biol. Chem. 1966, 241:1763-1768.
45. Muraguchi H., Kamada T. A mutation in the eln2 gene encoding a cytochrome P450 of Coprinus cinereus affects mushroom morphogenesis. Fungal Genet. Biol. 2000, 29:49-59.
46. Nelson D.R. The cytochrome P450 homepage. Hum. Genom. 2009, 4:59-65.
47. Ohm R.A., de Jong J.F., Lugones L.G., Aerts A., Kothe E., Stajich J.E., de Vries R.P., Record E., Levasseur A., Baker S.E., Bartholomew K.A., Coutinho P.M., Erdmann S., Fowler T.J., Gathman A.C., Lombard V., Henrissat B., Knabe N., Kues U., Lilly W.W., Lindquist E., Lucas S., Magnuson J.K., Piumi F., Raudaskoski M., Salamov A., Schmutz J., Schwarze F.W., vanKuyk P.A., Horton J.S., Grigoriev I.V., Wosten H.A. Genome sequence of the model mushroom Schizophyllum commune. Nat. Biotechnol. 2010, 28:957-963.
48. Pecyna M.J., Ullrich R., Bittner B., Clemens A., Scheibner K., Schubert R., Hofrichter M. Molecular characterization of aromatic peroxygenase from Agrocybe aegerita. Appl. Microbiol. Biotechnol. 2009, 84:885-897.
49. Perry C.R., Smith M., Britnell C.H., Wood D.A., Thurston C.F. Identification of two laccase genes in the cultivated mushroom Agaricus bisporus. J. Gen. Microbiol. 1993, 139(Pt 6):1209-1218.
50. Ruiz-Duenas F.J., Morales M., Garcia E., Miki Y., Martinez M.J., Martinez A.T. Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J. Exp. Bot. 2009, 60:441-452.
51. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., Sturn A., Snuffin M., Rezantsev A., Popov D., Ryltsov A., Kostukovich E., Borisovsky I., Liu Z., Vinsavich A., Trush V., Quackenbush J. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
52. Sakamoto Y., Nakade K., Sato T. Characterization of the post-harvest changes in gene transcription in the gill of the Lentinula edodes fruiting body. Curr. Genet. 2009, 55:409-423.
53. Shaw P.D., Hager L.P. Biological chlorination. III. beta-Ketoadipate chlorinase: a soluble enzyme system. J. Biol. Chem. 1959, 234:2565-2569.
54. Shiningavamwe A., Obiero G., Albertyn J., Nicaud J.M., Smit M. Heterologous expression of the benzoate para-hydroxylase encoding gene (CYP53B1) from Rhodotorula minuta by Yarrowia lipolytica. Appl. Microbiol. Biotechnol. 2006, 72:323-329.
55. Smith M., Shnyreva A., Wood D.A., Thurston C.F. Tandem organization and highly disparate expression of the two laccase genes lcc1 and lcc2 in the cultivated mushroom Agaricus bisporus. Microbiology 1998, 144(Pt 4):1063-1069.
56. Stajich J.E., Wilke S.K., Ahren D., Au C.H., Birren B.W., Borodovsky M., Burns C., Canback B., Casselton L.A., Cheng C.K., Deng J., Dietrich F.S., Fargo D.C., Farman M.L., Gathman A.C., Goldberg J., Guigo R., Hoegger P.J., Hooker J.B., Huggins A., James T.Y., Kamada T., Kilaru S., Kodira C., Kues U., Kupfer D., Kwan H.S., Lomsadze A., Li W., Lilly W.W., Ma L.J., Mackey A.J., Manning G., Martin F., Muraguchi H., Natvig D.O., Palmerini H., Ramesh M.A., Rehmeyer C.J., Roe B.A., Shenoy N., Stanke M., Ter-Hovhannisyan V., Tunlid A., Velagapudi R., Vision T.J., Zeng Q., Zolan M.E., Pukkila P.J. Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc. Natl. Acad. Sci. USA 2010, 107:11889-11894.
57. Steffen K.T., Hofrichter M., Hatakka A. Mineralisation of 14C-labelled synthetic lignin and ligninolytic enzyme activities of litter-decomposing basidiomycetous fungi. Appl. Microbiol. Biotechnol. 2000, 54:819-825.
58. Subramanian V., Yadav J.S. Role of P450 monooxygenases in the degradation of the endocrine-disrupting chemical nonylphenol by the white rot fungus Phanerochaete chrysosporium. Appl. Environ. Microbiol. 2009, 75:5570-5580.
59. Sugano Y., Matsushima Y., Tsuchiya K., Aoki H., Hirai M., Shoda M. Degradation pathway of an anthraquinone dye catalyzed by a unique peroxidase DyP from Thanatephorus cucumeris Dec 1. Biodegradation 2009, 20:433-440.
60. Sutherland J.B., Selby A.L., Freeman J.P., Evans F.E., Cerniglia C.E. Metabolism of phenanthrene by Phanerochaete chrysosporium. Appl. Environ. Microbiol. 1991, 57:3310-3316.
61. Syed K., Doddapaneni H., Subramanian V., Lam Y.W., Yadav J.S. Genome-to-function characterization of novel fungal P450 monooxygenases oxidizing polycyclic aromatic hydrocarbons (PAHs). Biochem. Biophys. Res. Commun. 2010, 399:492-497.
62. Thurston C.F. The structure and function of fungal laccases. Microbiology 1994, 140:19-26.
63. Turner E.M. Phenoloxidase activity in relation to substrate and development stage in the mushroom, Agaricus bisporus. Trans. Br. Mycol. Soc. 1974, 63:541-547.
64. Ullrich R., Hofrichter M. The haloperoxidase of the agaric fungus Agrocybe aegerita hydroxylates toluene and naphthalene. FEBS Lett. 2005, 579:6247-6250.
65. Ullrich R., Nuske J., Scheibner K., Spantzel J., Hofrichter M. Novel haloperoxidase from the agaric basidiomycete Agrocybe aegerita oxidizes aryl alcohols and aldehydes. Appl. Environ. Microbiol. 2004, 70:4575-4581.
66. van Gorcom R.F., Boschloo J.G., Kuijvenhoven A., Lange J., van Vark A.J., Bos C.J., van Balken J.A., Pouwels P.H., van den Hondel C.A. Isolation and molecular characterisation of the benzoate-para-hydroxylase gene (bphA) of Aspergillus niger: a member of a new gene family of the cytochrome P450 superfamily. Mol. Gen. Genet. 1990, 223:192-197.
67. Waksman S., Nissen W. On the nutrition of the cultivated mushroom Agaricus campestris, and the chemical changes brought about by this organism in the manure compost. Am. J. Bot. 1932, 19:514-537.
68. Waterman M.R., Lepesheva G.I. Sterol 14 alpha-demethylase, an abundant and essential mixed-function oxidase. Biochem. Biophys. Res. Commun. 2005, 338:418-422.
69. Whittaker J.W. The free radical-coupled copper active site of galactose oxidase. Metal Ions in Biological Sciences 1994, 315-360. Marcel Dekker, New York. H. Sigel, A. Sigel (Eds.).
70. Whittaker M.M., Kersten P.J., Nakamura N., Sanders-Loehr J., Schweizer E.S., Whittaker J.W. Glyoxal oxidase from Phanerochaete chrysosporium is a new radical-copper oxidase. J. Biol. Chem. 1996, 271:681-687.
71. Wood D.A. Inactivation of extracellular laccase during fruiting of Agaricus bisporus. J. Gen. Microbiol. 1980, 117:339-345.
72. Wood D.A., Goodenough P.W. Fruiting of Agaricus bisporus. Changes in extracellular enzyme activities during growth and fruiting. Arch. Microbiol. 1977, 114:161-165.
73. Yelle D.J., Ralph J., Lu F., Hammel K.E. Evidence for cleavage of lignin by a brown rot basidiomycete. Environ. Microbiol. 2008, 10:1844-1849.
74. 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. Identification and structural characterization of heme binding in a novel dyedecolorizing peroxidase, TyrA. Proteins 2007, 69:234-243.