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Computational and in Vitro Study of Isolated Domains from Fungal Polyketide Synthases

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Computational and in Vitro Study of Isolated Domains from Fungal Polyketide Synthases Computational and In Vitro Study of Isolated Domains from Fungal Polyketide Synthases Von der Naturwissenschaftlichen Fakultät der Gottfried Wilhelm Leibniz Universität Hannover zur Erlangung des Grades Doktor der Naturwissenschaften (Dr. rer. nat.) genehmigte Dissertation von Oliver Piech, M.Sc. 2020 Referent: Prof. Dr. Russell Cox Korreferent: Prof Dr. Plettenburg Tag der Promotion: 29.05.2020 ii Vi veri universum vivus vici iii Abstract Keywords: Polyketides, Enzyme engineering, Squalestatin tetrakeitde Synthase, Tenellin Diverse approaches have been explored to generate new polyketides by engineering polyketide synthases (PKS). Although it has been proven possible to produce new compounds by designed PKS, engineering strategies failed to make polyketides available via widely applicable rules and protocols. The aim of this work was the first rational engineering of an iterative highly- reducing polyketide synthase (HR-PKS). This approach was performed on the Squalestatin Tetraketide Synthase (SQTKS), which catalyses the biosynthesis of the tetraketide side chain of squalestatin-S1 53, which is a potent squalene synthase inhibitor and can be potentially used to treat serum cholesterol related diseases. Second, tenellin 62 was investigated, which is the product of the iterative Type I polyketide synthase non ribosomal peptide synthetase (PKS-NRPS) TENS. Using a combination of different in silico methods, structural models of the enoyl reductase (ER) domain of SQTKS were obtained and validated. With the generated protein models different rational engineering experiments in silico were performed, in which amino acids for the mutagenesis approach in vitro were identified. The subsequent in vitro experiments revealed that it was possible to rationally engineer the ER domain of SQTKS. In addition, the different integrated mutations showed different effects on the intrinsic programming of the ER domain. Further, the chemical selectivity and kinetic parameters of the tested di-, tri-, tetra- and heptaketide substrate were influenced in a specific way through the different mutated ER domains. In addition, the structural-biological foundations and analysis for the domain swaps between Pretenellin A Synthetase (TENS), Predesmethylbassianin A Synthetase (DMBS) and Premilitarinone C Synthetase (MILS) were investigated and validated. Through different in silico structural analyses it was possible to consider the effects of swaps on protein structure and to understand the effect of the swaps at the structural level. Additionally, the in silico analysis helped to clarify the influence of extrinsic and intrinsic programming factors. iv Kurzzusammenfassung Schlagwörter: Polyketide, Enzym engineering, Squalestatin tetrakeitde Synthase, Tenellin Verschiedene Ansätze wurden erforscht, um neue Polyketide durch engeeniering von Polyketide Synthasen (PKS) zu erzeugen. Obwohl es sich als möglich erwiesen hat neue Verbindungen durch künsltiche PKS herzustellen, erwieß es sich trotzdem nicht als möglich über allgemein anwendbare Regeln und Protokolle neue Polyketide herzustellen. Ziel dieser Arbeit war das erste rationale Engineering einer iterativen, hochreduzierenden Polyketid Synthase (HR-PKS). Dieser Ansatz wurde an der Squalestatin- Tetraketid-Synthase (SQTKS) durchgeführt, die die Biosynthese der Tetraketid-Seitenkette von Squalestatin-S1 53 katalysiert, einem wirksamen Inhibitor der Squalen-Synthase, der möglicherweise zur Behandlung von Erkrankungen im Zusammenhang mit Serumcholesterin eingesetzt werden kann. Desweiteren wurde Tenellin 62 untersucht, welches das Produkt der iterativen nicht-ribosomalen Peptid Synthetase (PKS-NRPS) TENS des Typ I ist. Unter Verwendung einer Kombination verschiedener in silico Methoden wurde ein Strukturmodell der Enoylreduktase (ER) Domäne von SQTKS erzeugt und validiert. Mit den generierten Proteinmodellen wurden verschiedene rationale Engineering Experimente in silico durchgeführt, wobei unteranderem Aminosäuren für den in vitro Mutageneseansatz identifiziert wurden. Die anschließenden in-vitro Experimente zeigten, dass es möglich war, die ER-Domäne von SQTKS rational zu engeenieren. Darüber hinaus zeigten die verschiedenen generierten Mutationen unterschiedliche Auswirkungen auf die intrinsische Programmierung der ER- Domäne. Darüber hinaus wurden die chemische Selektivität und die kinetischen Parameter des getesteten Di-, Tri-, Tetra- und Heptaketisubstrate auf spezifische Weise durch die verschiedenen mutierten ER-Domänen beeinflusst. Darüber hinaus wurden die strukturbiologischen Grundlagen und Analysen für die Domain- Swaps zwischen Pretenellin-A-Synthetase (TENS), Predesmethylbassianin-A-Synthetase (DMBS) und Premilitarinon-C-Synthetase (MILS) untersucht und validierd Durch verschiedene in silico Strukturanalysen konnten die Auswirkungen von Swaps auf die Proteinstruktur berücksichtigt und die Auswirkungen der Swaps auf die Strukturebene verstanden werden. Darüber hinaus hat die in silico-Analyse dazu beigetragen, den Einfluss extrinsischer und intrinsischer Faktoren der Programmierung zu klären. v Acknowledgements I would like to thank Prof. Russell Cox for providing me with such an interesting project to work on, and for his thorough and dedicated supervision throughout the course of my PhD. His support and encouragement was highly appreciated. Especially, I would like to thank Prof Plettenburg taking the time to be the co-referee and chair of the examination board of my PhD thesis. No, less I thank Prof Preller for beeing examiner. I would like to thank all past and current Cox group members, in particular, Verena, Karen, Haili, Francesco, Eric, Katja, Lukas, Carsten and my master student Yingwen Wu. Beate Bonsch and Christoph Bartels, who give me an affectionate reception into the group. At last, my office member Vjaceslavs Hrupins, who made the time enjoyable. In addition, once more Carsten and Lukas for all the time, we spent playing billard or were drinking beer and Eric, which whom I spend a great time in China on a holiday. Furthermore, from the other groups of the OCI/BMWZ Maik Siebke, for all the Döner we eat together. Wiebke Hutwelker and Simon Blazy whom became good friends over the time and made the time very enjoyable. Lukas Schaaf whom also became a good friend and for all the time we drank whiskey together. I want to thank Michael Ringel, who helped me a great deal with the SPR measurements. Also Tjorven Ostermeier and Luca Codutti, for the help with the ITC measurements. I also want to thank the members of the OCI and BMWZ. Especially the members of the NMR and MS department and the members of the media kitchen. Katja Körner and Anika Shaperjahn, who also did a great deal of work and without this contribution my research, would be not this fast. I want to thank my friends outside the OCI and BMWZ in Hannover, Nina Bornemann, Philipp Müller and Sandra Dienemann. Sabrina Czelusteck, for the last beautiful years. Finally, my family for their help and support during my studies and that you are there if I need you. vi Table of contents Abstract................................................................................................................................. iv Kurzzusammenfassung ...................................................................................................... v Acknowledgements ............................................................................................................ vi List of Abbreviations and Units ........................................................................................ xi 1 Introduction ................................................................................................................... 1 1.1 Natural Products ........................................................................................................1 1.2 Fatty Acid Biosynthesis ..............................................................................................2 1.3 Enzymes of Fatty Acid Biosynthesis ............................................................................3 1.4 Architecture of Fatty Acid Synthases ..........................................................................7 1.5 From Fatty Acid Synthases (FAS) to Polyketide Synthases (PKS)..................................8 1.6 Biosynthesis of Polyketides ........................................................................................9 1.6.1 Mechanism of the C-MeT domain in PKS ................................................................. 11 1.7 Polyketide Synthases ............................................................................................... 11 1.8 Modular Type I Polyketide Synthases ....................................................................... 12 1.9 Iterative Type I Polyketide Synthases ....................................................................... 14 1.10 Highly Reducing Iterative Polyketide Synthase (HR-PKS)........................................... 15 1.11 Stereochemical course in HR-PKS ............................................................................. 17 1.11.1 Excursus into KR domains ..................................................................................... 19 1.12 Biosynthesis of Squalestatin Tetraketide Synthase ................................................... 21 1.13 Biosynthesis of Tenellin ........................................................................................... 23 1.14 Engineering of Polyketide Synthases .......................................................................
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