Genetic Potential of Lichen-Forming Fungi in Polyketide Biosynthesis

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Genetic Potential of Lichen-Forming Fungi in Polyketide Biosynthesis Genetic Potential of Lichen-Forming Fungi in Polyketide Biosynthesis A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Yit Heng Chooi B.Sc. (Hons) School of Applied Sciences Science, Engineering and Technology Portfolio RMIT University March 2008 Declaration The work presented in this thesis was completed in the period of August 2004 to March 2008 under the co-supervision of Assoc. Professor Ann Lawrie and Professor David Stalker at School of Applied Sciences, RMIT University, and Dr. Simone Louwhoff at Royal Botanical Gardens, Victoria. In compliance with the university regulatioins, I declare that: I. except where due acknowledgement has been made; the work is that of the author alone II. the work has not been submitted previously, in whole or in part, to qualify for any other academic award; III. the content of the thesis is the result of work which has been carried out since the official commencement date of the approved research program; IV. ethics procedures and guidelines have been followed. _________________ Yit Heng Chooi 27th March 2008 II Dedication To my parents and my beloved wife Lee Ngoh III Acknowledgement There are many individuals without whom the work described in this thesis might not have been possible, and to whom I am greatly indebted. I would like to thank my supervisor Associate Professor Ann Lawrie for, firstly, the opportunity to undertake this research topic of my own interest, and for her guidance, patience, and encouragement in the most challenging times. I would also like to express my sincere thanks to both of my co-supervisors. To Professor David Stalker who has taught me the true spirit of research, and to Dr. Simone Louwhoff who has introduced me to the beautiful world of lichenology. I am very grateful to RMIT University for providing the RMIT Malaysia-Australia Colombo plan Commemoration (MACC) Scholarship. I am deeply indebted to Emeritus Professor Jack Elix at the Department of Chemistry, Australian National University for his assistance in chemical analysis, for proofreading the introductory part of my thesis and for having been an extremely supportive and generous mentor. His insights into the mechanisms of organic reactions and his wealth of knowledge on lichens and their secondary metabolites have been crucial in my research, and his enthusiasm and passion in science and teaching has been truly inspirational. I would like to express my gratitude to Professor Isao Fujii and Professor Yutaka Ebizuka at the Graduate School of Pharmaceutical Sciences, The University of Tokyo for the opportunity to work with a group of vibrant scientists at the forefront of natural product research, for the valuable contributions of time and materials, and for their generous advice and guidance (Prof. Fujii is now at School of Pharmacy, Iwate Medical University). Although the research visit has only lasted for five weeks, I have learnt a lot from the people in the lab and the experience was invaluable for my scientific career development. A special thanks to Dr. Tetsuo Kushiro and Dr. Yasuyo Seshime, Takayuki Itoh, Tomohiro Moriya, Tomomi Moriguchi, Natsuki Nambu and Hiroki Sano, for their assistance in my experiments and made my stay in Tokyo enjoyable. I am also very grateful to T. Itoh, T. Kushiro, I. Fujii and Y. Ebizuka for communicating their unpublished results. IV Similarly, I am very grateful to Associate Professor Meryl Davis at the Genetics Deparment, University of Melbourne for her contribution of ideas and encouragement and for providing the Aspergillus nidulans strain, plasmid and other resources. I would also like to thank David Clarke at University of Melbourne for his assistance in A. nidulans transformation. Associate Professor Daniele Armaleo at the Department of Biology, Duke University is also thanked for his constructive suggestions and for communicating unpublished results. Those who aided me in the lab; I thank Dr. Gregory Nugent, who was then a post- doc but is now a lecturer in the department, and Dr. Brian Meehan, for always being there to give me the appropriate advice and encouragement. I would also like to thank my friends and colleagues in the lab and department for their company, friendship and support. In particular to Kavitha who is now a proud mother, for the long hours spent together over failed Southern blotting and difficult cloning, and made the journey fun. I would like to thank my parents for believing in me and for being proud of me. Their unconditional love and support has given me the strength and courage while I am away from home. Most importantly, I would like to thank my wife Lee Ngoh, for being the most patient and supportive witness to my academic journey over the past three and a half years. Without her support, love and encouragement, this study would not have been possible. V TABLE OF CONTENTS Title Page I Declaration II Dedication III Acknowledgement IV Table of Contents VI List of Figures XI List of Tables XIX List of Abbreviations XXI Publications XXIII Abstract XXIV CHAPTER 1 INTRODUCTION AND BACKGROUND 1 1.1 Introduction 2 1.2 Background 5 1.2.1 The lichens 5 1.2.2 Chemistry and lichens 7 1.2.3 Lichen secondary metabolites 9 1.2.3.1 The biological significance of lichen metabolites 13 1.2.3.2 Chemotaxonomy of lichens 13 1.2.4 Prospects and applications of lichen natural products 14 1.2.4.1 Pharmacology and medicine 14 1.2.4.2 Potential applications in agriculture 18 1.2.4.3 Cosmetics and perfume industry 19 1.2.5 The polyketide factories 20 1.2.6 The unique lichen compounds and the ubiquitous PKSs 27 1.2.6.1 Lichen polyketides common to other fungi 28 1.2.6.2 Polyketide compounds common in lichens 30 1.2.6.2.1 Basic monoaromatic units that form lichen coupled phenolics 33 1.2.6.2.2 The formation of various linkages in lichen coupled phenolics 37 1.2.6.2.3 Derivatization of the basic monoaromatic units 39 1.2.6.2.4 Depsides 43 1.2.6.2.5 Depsidones 50 1.2.6.2.6 Diphenyl ethers 56 1.2.6.2.7 Depsones 61 1.2.6.2.8 Dibenzofurans and usnic acid homologs 63 1.2.6.2.9 Biphenyls 67 1.2.6.3 Lichens as combinatorial chemists 68 1.3 Research scope and objectives 75 VI CHAPTER 2 COMMON MATERIALS AND METHODS 76 2.1 Introduction 77 2.2 Molecular biology techniques 77 2.2.1 Small-scale lichen DNA extraction 77 2.2.2 Large-scale lichen DNA extraction 77 2.2.3 Polymerase chain reaction (PCR) 78 2.2.4 Gel electrophoresis (GE) 80 2.2.5 DNA purification and gel extraction 81 2.2.6 DNA sequencing 81 2.2.7 Plasmid miniprep 81 2.2.8 Transformation of Escherichia coli by electroporation 82 2.2.9 Colony-direct PCR 82 2.2.10 Cloning of PCR products 82 2.2.11 Restriction digestion and ligation of DNA 83 2.2.12 Southern blotting 83 2.3 Bioinformatic analysis 83 2.3.1 Raw sequence editing 83 2.3.2 Multiple sequence alignment and phylogenetic analysis 84 2.3.3 Gene annotation and plasmid map drawing 86 2.3.4 Drawing of chemical structures 86 CHAPTER 3 DIVERSITY OF POLYKETIDE SYNTHASE GENES IN 87 LICHENS 3.1 Introduction 89 3.1.1 Exploring the genetic diversity of fungal PKSs 89 Correlating the structure of polyketides and PKS genes with 3.1.2 phylogenetic analysis 93 3.1.3 Research goals 96 3.2 Lichen identification and chemical analysis 97 3.2.1 Materials and methods 97 3.2.1.1 Lichen collection and identification 97 3.2.1.2 Thin layer chromatography (TLC) 98 3.2.1.3 High performance liquid chromatography (HPLC) 98 3.2.1.4 PCR amplification of internal transcribed spacer regions 99 3.2.2 Results 99 3.2.2.1 Lichen specimens and identification 99 3.2.2.2 Chemical analysis of lichens 105 3.2.2.3 Internal transcribed spacer (ITS) regions 111 3.2.3 Discussion 112 VII 3.3 NR- and PR-type KS domain-specific degenerate 113 primers 3.3.1 Materials and methods 114 3.3.1.1 Design of degenerate primers 114 3.3.1.2 PCR amplification of KS domain 114 3.3.1.3 KS domain sequence analysis 114 3.3.2 Results 115 3.3.2.1 NRKS degenerate primers 115 3.3.2.2 PRKS degenerate primers 115 3.3.2.3 PCR results and KS domain sequence analyses 118 3.3.3 Discussion 120 3.3.3.1 NRKS amplified KS domains 121 3.3.3.2 PRKS amplified KS domain 121 3.4 Clade III NR-type KS domain-specific degenerate 124 primers 3.4.1 Materials and methods 125 3.4.1.1 Design of degenerate primers 125 3.4.1.2 PCR amplification of KS domain and sequence analysis 125 3.4.2 Results 125 3.4.2.1 NR3KS degenerate primers 125 3.4.2.2 PCR results and KS domain sequence analyses 127 3.4.3 Discussion 128 3.5 Phylogenetic analysis of lichen KS domains 130 3.5.1 Materials and methods 131 3.5.1.1 Multiple sequence alignment 131 3.5.1.2 Construction of phylogenetic tree 131 3.5.2 Results 132 3.5.3 Discussion 134 3.5.3.1 Non-reducing PKS Clade I 134 3.5.3.2 Non-reducing PKS Clade II 139 3.5.3.3 Non-reducing PKS basal to Clades I and II 142 3.5.3.4 Non-reducing PKS Clade III 143 3.5.3.5 Partial-reducing PKSs 147 3.5.3.6 Highly-reducing PKSs 148 3.6 Conclusions and overview 149 CHAPTER 4 LOCATING AND CLONING LICHEN PKS GENES 153 4.1 Introduction 155 4.1.1 Rationale and research goal 160 4.2 Locating and cloning of partial PKS genes in 161 Flavoparmelia caperatulla 4.2.1 Materials and methods 162 4.2.1.1 Southern blotting 162 4.2.1.2 Construction of partial genomic library 162 VIII 4.2.1.3 Screening of partial genomic library 163 4.2.2 Results 163 4.2.2.1 Southern blotting 163 4.2.2.2 Construction and screening of partial genomic library 165 4.2.3 Discussion 167 4.2.3.1 High molecular weight lichen DNA for Southern and cloning 167 4.2.3.2 Southern-guided library construction and PCR screening 168 4.3 Locating and cloning of partial PKS genes in 170 Xanthoparmelia semiviridis 4.3.1 Materials and methods 170 4.3.1.1 Southern blotting 171 4.3.1.2 Construction of X.
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