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Biosynthesis of Fungal Alkyl Citrates and Polyketides

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Biosynthesis of Fungal Alkyl Citrates and Polyketides Biosynthesis of Fungal Alkyl Citrates and Polyketides Von der Naturwissenschaftlichen Fakultät Gottfried Wilhelm Leibniz Universität Hannover zur Erlangung des Grades Doktor der Naturwissenschaften (Dr. rer. nat.) genehmigte Dissertation von Sen Yin, Master (China) 2020 Referent: Prof. Dr. Russell Cox Korreferent: Prof. Dr. Andreas Kirschning Tag der Promotion: 02.10.2020 Abstract Abstract The main focus of the presented work concentrated on understanding the biosynthetic pathway of viridofungin, exploring the enzymatic properties of the key enzymes from the byssochlamic acid pathway, and engineering the PKS of tenellin. In a combined genetic and chemical approach, the biosynthetic pathway of viridiofungin and functions of enzymes from of byssochlamic acid pathway and programming of the tenellin PKS (TENS) system were elucidated. Trichoderma viride MF5628 was firstly genome sequenced by Illumina and Oxford nanopore sequencing. Then, using a combination of targeted gene knockout and RNA interference-based silencing in the native organism, a novel unreported tRNA ligase like enzyme involved in the biosynthetic pathway was identified. A citrate synthase like enzyme and a tRNA ligase like enzyme were found to be essential to the biosynthesis of viridiofungin. The biosynthesis of byssochlamic acid was investigated by protein expression and in vitro study. A hydrolase, citrate synthase, two 2-methyl citrate dehydratases, two KSI and two PEBP proteins were expressed in E. coli or yeast, in addition, in vtiro assay was carried out by using these proteins. During maleic anhydride monomer biosynthesis, a hydrolase can hydrolyze the hexaketide from ACP. Citrate synthase can use hexaketide CoA and oxaloacetate as substrates to form (2S, 3R) citrate. 2-Methyl citrate dehydratase takes (2S, 3R) citrate diasteroisomer as substrate to form a 2, 3-alkene product, and the product can spontaneously form a cyclised maleic anhydride monomer. Two KSI finally used maleic anhydride monomer to form the dimerised product byssochlamic acid. Two PEBP enzymes are not thought to be involved in catalysis of dimerization. Based on KR domain swap experiment on TenS, chain-length programming in TenS was elucidated. Six KR domain subfragments were swapped with the homologous fragments from hexaketide desmethylbassianin synthase (DMBS) and three with the heptaketide militarinone synthase (MILS) resulted in the synthesis of different chain length of polyketide products. Particularly, the MILS KR domain swap resulted in the synthesis of penta, hexa and heptaketides. The results of these and previous experiments in our group are rationalised by considering the existence of competition between the C-MeT and KR domains. Keywords: viridiofungin, byssochlamic acid, biosynthesis, PKS, domain swap i Abstract Zusammenfassung Das Hauptaugenmerk der vorgestellten Arbeit lag auf dem Verständnis des Biosynthesewegs von Viridofungin, der Untersuchung der enzymatischen Eigenschaften der Schlüsselenzyme aus dem Byssochlaminsäure-Weg und der Entwicklung der PKS von Tenellin. In einer kombination aus genetischen und chemischen experimenten Ansatz wurden der Biosyntheseweg von Viridiofungin und die Funktionen von Enzymen aus dem Byssochlaminsäure-Weg sowie die Programmierung des Tenellin-PKS (TENS) -Systems aufgeklärt. Das Trichoderma-virid MF5628 wurde zunächst durch Illumina- und Oxford-Nanoporen- Sequenzierung genomsequenziert. Es wurde unter Verwendung einer Kombination aus gezielter Gen-Knockout- und RNA-Interference-basierter Stummschaltung im nativen Organismus ein neuer, nicht veröffentlicht Biosyntheseweg identifiziert, an dem eine tRNA-Ligase beteiligt ist. Es wurde festgestellt, dass ein Citrat-Synthase-ähnliches Enzym und ein tRNA-Ligase-ähnliches Enzym für die Biosynthese von Viridiofungin essentiell sind. Die Biosynthese von Byssochlaminsäure wurde durch Proteinexpression und in-vitro- Studie enukleiert. Eine Hydrolase, Citrat-Synthase, zwei 2-Methylcitrat-Dehydratase, zwei KSIs und zwei PEBPs-Proteine wurden in E. coli und Hefe exprimiert. Während der Maleinsäureanhydridmonomer Biosynthese kann eine Hydrolase die Hexaketidform vom ACP hydrolysieren. Die Citrat-Synthase kann Hexaketid-CoA und Oxalacetat als Substrat verwenden, um (2S, 3R) -Citrat zu bilden. 2-Methylcitrat-Dehydratase nimmt (2S, 3R) -Citrat-Diasteroisomer als Substrat, um ein 2, 3-Alken im Produkt zu bilden, und das Produkt kann ein spontan cyclisiertes Maleinsäureanhydridmonomer bilden. Zwei KSI verwenden schließlich Maleinsäureanhydrid-monomer, um das dimerisierte Produkt Byssochlaminsäure zu bilden. PEBP-Enzyme sind nicht der Katalyse der Dimerisierung beteiligt. Basierend auf dem KR-Domain-Swap-Experiment mit TenS wurde die Kettenlängenprogrammierung in TenS aufgeklärt. Sechs KR-Domänen-Subfragmente, die mit den homologen Fragmenten der Hexaketid-Desmethylbassianin-Synthase (DMBS) und drei mit der Heptaketid-Militarinon-Synthase (MILS) ausgetauscht wurden, führten zur Synthese unterschiedlicher Kettenlängen von Polyketid-Produkten. Insbesondere der MILS KR- Domänenaustausch führte zur Synthese von Penta, Hexa und Heptaketiden. Die Ergebnisse dieser und vorherger Experimente in unserer Gruppe werden einbezogen, indem die Existenz einer Konkurrenz zwischen den CMeT- und KR-Domänen berücksichtigt wird. Schlüsselwörter: viridiofungin, byssochlamic acid, Biosynthese, PKS, domain-swap ii Acknowledgement Acknowledgement Thanks, Prof. Russell Cox for giving me the opportunity to finish my PhD in this fantastic group. I appreciate your professional supervision and kind help throughout the last four years. Thanks, all cooperation partners the CeBiTEC Bielefeld, especially Prof Jörn Kalinowski and Dr Daniel Wibberg; thanks Prof. Jianqiang Kong for yeast expression strain and vectors. Thanks, BMWZ media kitchen team, especially to Katja; OCI colleague Dr Jörg Fohrer and Dr Gerald Dräger for their help with NMR and mass related matters. Thanks, our group members (Liz, Dongsong, Chongqing, Steffen, Jin, Lei, Yunlong, Slawik, Erik, Hao, Carsten, Karen, Lukas, Oliver, Mary, Eman, Raissa, Verena …). Thanks, China Scholarship Council (CSC) for the foundation. Thanks, my parents who always covered my back in my life. Submitting this thesis is only possible because of you. iii Abbreviations and units Abbreviations and Units AA amino acid KR β-ketoreductase ACP acyl carrier protein ΨKR pseudo-ketoreductase acetyl-CoA acetyl-coenzyme A LCMS liquid chromatography mass spectrometry AntiSMAS antibiotic and Secondary Metabolite Analysis H Shell DAD diode-array detection AT acyltranferase MCoA malonyl-CoA att site-specific attachment MeOD deuterated methanol bp base pair MeOH methanol BLAST basic local alignment search tool MS mass spectrometry CDCl3 deuterated chloroform MeT methyltransferase cDNA copy deoxyribonucleic acid MAT malonyl/acetyl tranferase C-Met C-methyltrasferase mFAS mammalian fatty acid synthase CoASH coenzyme A mRNA messeinger ribonucleic acid NAD(P) nicotinamide adenine dinucleotide CS citrate synthase H (phosphate) COSY homonuclear correlation spectroscopy NOESY nuclear overhauser effect spectroscopy dATP deoxyadenosine triphosphate NPRS nonribosomal peptide synthetase DH dehydratase NMR nuclear magnetic resonance DNA deoxyribonucleic acid nr-iPKS nonreducing iterative PKS ELSD evaporative light scattering detector ORF open reading frame ESI electrospray ionization PamyB AmyB promoter ER enoyl reductase PgpdA GpdA promoter FAS fatty acid synthase PCR polymerase chain reaction FAD flavin adenine dinucleotide PKS polyketide synthase gDNA genomic DNA pr-iPKS partially reducing iterative PKS HMBC heteronuclear multiple bond correlation RNA ribonucleic acid HRAM high resolution accurate mass RT retention time 1H NMR proton NMR SAM S-adenosyl-methionine HPLC high performance liquid chromatography SAT starter unit: ACP transacylase hr-iPKS highly reducing iterative PKS SM secondary metabolite HRMS high resolution molecular weight TE thiolesterase HSQC heteronuclear single quantum coherence tf transformant ITS internal transcribed spacer TIC total ion current iPKS iterative PKS UV ultraviolet KS ketosynthase WT wild-type iv Contents Contents Abstract .......................................................................................................................................... i Zusammenfassung .........................................................................................................................ii Acknowledgement ........................................................................................................................ iii Abbreviations and Units ................................................................................................................ iv Chapter 1. Introduction and Background of the Projects ...................................................... 1 1.1 General overview of projects. ............................................................................................. 1 1.2 Natural products, secondary metabolites and their major classes. ................................... 2 1.3 Polyketides and Fatty acids. ................................................................................................ 4 1.3.1 Basic enzymology of polyketide and fatty acid biosynthesis. ...................................... 4 1.3.1.1 Acyl transfer. ............................................................................................. 4 1.3.1.2 Condensation step. ..................................................................................
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