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The White-Rot Fungi Phlebia Radiata and Dichomitus Squalens in Wood-Based Cultures: Expression of Laccases, Lignin Peroxidases, and Oxalate Decarboxylase

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The White-Rot Fungi Phlebia Radiata and Dichomitus Squalens in Wood-Based Cultures: Expression of Laccases, Lignin Peroxidases, and Oxalate Decarboxylase The white-rot fungi Phlebia radiata and Dichomitus squalens in wood-based cultures: expression of laccases, lignin peroxidases, and oxalate decarboxylase Miia R. Mäkelä Department of Applied Chemistry and Microbiology Division of Microbiology Faculty of Agriculture and Forestry and Viikki Graduate School in Molecular Biosciences University of Helsinki ACADEMIC DISSERTATION To be presented, with the permission of the Faculty of Agriculture and Forestry of the University of Helsinki, for public criticism in Auditorium B2 (A109), Latokartanonkaari 7, on December 4th 2009, at 12 o’clock noon. Helsinki 2009 Supervisors: Docent Taina Lundell Department of Applied Chemistry and Microbiology University of Helsinki Finland Professor Annele Hatakka Department of Applied Chemistry and Microbiology University of Helsinki Finland Reviewers: Professor Leif J. Jönsson Department of Chemistry Umeå University Umeå, Sweden Docent Markku Saloheimo VTT Espoo, Finland Opponent: Professor Ursula Kües Institute of Forest Botany University of Göttingen Göttingen, Germany Printed Yliopistopaino, Helsinki, Finland Layout Timo Päivärinta ISSN 1795-7079 ISBN 978-952-10-5890-5 (paperback) ISBN 978-952-10-5891-2 (PDF) Front cover White-rotted wood (photo: Miia Mäkelä) Contents List of original publications Author’s contribution Abbreviations Abstract Tiivistelmä (Abstract in Finnish) 1 Introduction .................................................................................................................1 1.1 Wood composition ..................................................................................................1 1.2 Wood degradation by fungi .....................................................................................3 1.3 Lignin-modifying enzymes .....................................................................................4 1.3.1 Lignin-modifying peroxidases ......................................................................5 1.3.1.1 Occurrence and properties of lignin-modifying peroxidases ............5 1.3.1.2 Catalytic reactions of lignin-modifying peroxidases .........................6 1.3.1.3 Evolutional relations of lignin-modifying peroxidases .....................7 1.3.1.4 Regulation of lignin-modifying peroxidase expression ....................7 1.3.2 Laccase ..........................................................................................................8 1.3.2.1 Biochemical and molecular properties of fungal laccases ................9 1.3.2.2 Roles of fungal laccases ..................................................................11 1.3.2.3 Fungal laccase genes .......................................................................11 1.3.2.4 Regulation of laccase-encoding expression ....................................12 1.4 Fungal degradation of wood polysaccharides .......................................................12 1.4.1 Enzymatic decomposition of cellulose ........................................................12 1.4.2 Non-enzymatic decomposition of cellulose .................................................13 1.4.3 Decomposition of hemicellulose by basidiomycetous fungi .......................14 1.5 Fungal low molecular weight compounds and wood degradation .......................15 1.6 Organic acids secreted by wood-decaying fungi ..................................................16 1.6.1 Oxalic acid ...................................................................................................16 1.6.1.1 Fungal synthesis of oxalic acid .......................................................16 1.6.1.2 Roles of fungal-produced oxalic acid ..............................................17 1.6.2 Oxalic-acid degrading enzymes ...................................................................20 1.6.3 Oxalate decarboxylase .................................................................................21 1.7 Basidiomycete genomes and lignocellulose decay ...............................................25 1.8 Phlebia radiata .....................................................................................................27 1.9 Dichomitus squalens .............................................................................................30 1.10 White-rot fungi and their enzymes in biotechnological applications..................32 2 Objectives of the study ..............................................................................................35 3 Materials and methods .............................................................................................36 3.1 Cultivation of Phlebia radiata ..............................................................................36 3.2 Purifi cation of P. radiata laccases .........................................................................37 3.3 Cultivation of Dichomitus squalens ......................................................................38 3.4 Cloning and expression of D. squalens laccases...................................................38 4 Results and discussion ..............................................................................................39 4.1 Characterization and expression of Phlebia radiata lignin peroxidase encoding genes (I) .................................................................................................39 4.2 Characterization and expression of P. radiata laccase-encoding genes (II) .........40 4.2.1 P. radiata Lac1 and Lac2 encoding genes and proteins ...............................40 4.2.2 Expression of P. radiata laccase transcripts ................................................41 4.3 Effect of copper and nitrogen supplements on submerged cultures of P. radiata 43 4.3.1 P. radiata laccase production .......................................................................43 4.3.2 Production of lignin-modifying peroxidases by P. radiata ..........................46 4.4 Laccases of Dichomitus squalens .........................................................................47 4.4.1 Production of laccases by D. squalens .........................................................48 4.4.2 Laccase-encoding genes of D. squalens ......................................................49 4.5 Production of oxalate decarboxylase and organic acids in wood-decaying white-rot fungi (III) .....................................................................50 4.5.1 Oxalate decarboxylase activity ....................................................................50 4.5.2 Secretion of organic acids ............................................................................51 4.6 Oxalate decarboxylase of D. squalens (IV) ..........................................................52 4.6.1 Characteristics of D. squalens oxalate decarboxylase .................................52 4.6.2 Activity and expression of D. squalens oxalate decarboxylase ...................54 5 Summary and conclusions ........................................................................................56 6 Acknowledgements ....................................................................................................58 7 References ..................................................................................................................59 List of original publications This thesis is based on the following publications, which are referred in the text by Roman numerals I-IV. In addition, unpublished data is presented. I Hildén, K.S., Mäkelä, M.R., Hakala, T.K., Hatakka, A. and Lundell, T. 2006. Expression on wood, molecular cloning and characterization of three lignin peroxidase (LiP) encoding genes of the white rot fungus Phlebia radiata. Current Genetics 49, 97-105. II Mäkelä, M.R., Hildén, K.S., Hakala, T.K., Hatakka, A. and Lundell, T.K. 2006. Expression and molecular properties of a new laccase of the white rot fungus Phlebia radiata grown on wood. Current Genetics 50, 323-333. III Mäkelä, M., Galkin, S., Hatakka, A. and Lundell, T. 2002. Production of organic acids and oxalate decarboxylase in lignin-degrading white rot fungi. Enzyme and Microbial Technology 30, 542-549. IV Mäkelä, M.R., Hildén, K., Hatakka, A. and Lundell, T.K. 2009. Oxalate decarboxylase of the white-rot fungus Dichomitus squalens demonstrates a novel enzyme primary structure and non-induced expression on wood and in liquid cultures. Microbiology 155, 2726-2738. The original publications are reprinted with the kind permission of the copyright holders. Author’s contribution I The author participated in planning and conducting the laboratory work, in particular in RT-PCR, gene expression and cloning. She did the fungal submerged and semi-solid cultivations and measured enzyme activities. She collaborated in the analysis and the interpretation of the results, and the writing of the article. II The author planned the experiments and did the laboratory work except for the solid wood cultivation. She did the phylogenetic analysis together with T. Lundell. The author analysed and interpreted the results and wrote the article. III The author planned the experiments, did the laboratory work except for the HPLC analysis. CZE method used in this work was developed by S. Galkin. The author analysed and interpreted the results, and took principal action in writing the article. IV The author planned the experiments and did the laboratory work. She did the phylogenetic analysis together with T. Lundell. The author analysed and interpreted the results and wrote the article. Abbreviations AAO aryl alcohol oxidase ATP adenosine triphosphate bp
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