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Metabolomic and Genomic Investigation Into the Actinomycete Genus Planomonospora

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Metabolomic and Genomic Investigation Into the Actinomycete Genus Planomonospora UvA-DARE (Digital Academic Repository) Metabolomic and genomic investigation into the actinomycete genus Planomonospora Zdouc, M.M. Publication date 2021 Document Version Final published version Link to publication Citation for published version (APA): Zdouc, M. M. (2021). Metabolomic and genomic investigation into the actinomycete genus Planomonospora. General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:09 Oct 2021 Metabolomic and Genomic Investigation into the Actinomycete Genus Metabolomic and Genomic Investigation into the Actinomycete Genus Planomonospora Planomonospora Mitja M. Zdouc Mitja M. Zdouc Metabolomic and Genomic Investigation into the Actinomycete Genus Planomonospora ACADEMISCH PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit van Amsterdam op gezag van de Rector Magnificus prof. dr. ir. K.I.J. Maex ten overstaan van een door het College voor Promoties ingestelde commissie, in het openbaar te verdedigen op maandag 28 juni 2021, te 14.00 uur door Mitja Maximilian Zdouc geboren te Klagenfurt Promotiecommissie Promotor: dr. T. den Blaauwen Universiteit van Amsterdam Copromotores: dr. M. Sosio NAISCONS prof. dr. L.W. Hamoen Universiteit van Amsterdam Overige leden: prof. dr. G.P. van Wezel Universiteit Leiden prof. dr. L.W. Hamoen Universiteit van Amsterdam prof. dr. J. Hugenholtz Universiteit van Amsterdam dr. M.A. Fernández Ibáñez Universiteit van Amsterdam dr. J.J.J. van der Hooft Wageningen University & Research prof. dr. C.R. Berkers Universiteit Utrecht Faculteit der Natuurwetenschappen, Wiskunde en Informatica II III Copyright © 2020 Mitja Maximilian Zdouc. All rights reserved. No part of this publication may be reproduced in any form without permission from the author. The studies described in this thesis were carried out at in the research laboratories of Naicons Srl in Viale Ortles 22/4, 20139 Milan, Italy and at the Institut für Pharmazeutische Biologie, Rheinische Friedrich-Wilhelms-Universität, Nußallee 6, 53115 Bonn, Germany. Mitja Maximilian Zdouc was financially supported by the European Union’s Horizon 2020 research and innovation program under grant agreement No.721484 (Train2Target). Cover Design: The cover shows an electron microscope scan of Planomonospora parontospora ATCC 23863. Image taken from the Digital Atlas of Actinomycetes (http://atlas.actino.jp/), with courtesy of the Society for Actinomycetes Japan. Image by G. Vobis, from Thiemann et al. 1967, 15, 27-38. IV Table of Contents LIST OF ABBREVIATIONS VII GENERAL INTRODUCTION 1 1.1 NATURAL PRODUCT PRODUCERS: ACTINOMYCETES 4 1.1.1 RARE ACTINOMYCETES 6 1.2 ACTINOMYCETE GENETICS 8 1.3 GENOMICS AND METABOLOMICS IN THE FIELD OF NATURAL PRODUCTS 16 1.4 SCOPE OF THE THESIS 21 1.5 REFERENCES 22 CREATION OF AN IN SILICO MS2 FRAGMENTATION LIBRARY FOR AUTOMATED DEREPLICATION 31 2.1 ABSTRACT 32 2.2 INTRODUCTION 33 2.3 RESULTS & DISCUSSION 35 2.4 CONCLUSION 40 2.5 ACKNOWLEDGEMENTS 42 2.6 EXPERIMENTAL SECTION 42 2.7 REFERENCES 43 2.8 SUPPLEMENTAL INFORMATION 45 PLANOMONOSPORA: A METABOLOMICS PERSPECTIVE ON AN UNDEREXPLORED ACTINOBACTERIA GENUS 47 3.1 ABSTRACT 48 3.2 INTRODUCTION 49 3.3 RESULTS & DISCUSSION 51 3.4 CONCLUSION 70 3.5 AUTHOR CONTRIBUTIONS & NOTES 71 3.6 ACKNOWLEDGEMENTS 71 3.7 EXPERIMENTAL SECTION 72 3.8 REFERENCES 76 3.9 SUPPLEMENTAL INFORMATION 84 A BIARYL-LINKED TRIPEPTIDE FROM PLANOMONOSPORA REVEALS A WIDESPREAD CLASS OF MINIMAL RIPP GENE CLUSTERS 117 4.1 ABSTRACT 118 4.2 INTRODUCTION 119 V 4.3 RESULTS & DISCUSSION 120 4.4 CONCLUSION 129 4.5 AUTHOR CONTRIBUTIONS 129 4.6 ACKNOWLEDGEMENTS 130 4.7 EXPERIMENTAL SECTION 130 4.8 REFERENCES 134 4.9 SUPPLEMENTAL INFORMATION 137 GENERAL DISCUSSION 151 5.1 REFERENCES 158 SUMMARY 159 SAMENVATTING 163 ZUSAMMENFASSUNG 167 POVZETEK 171 ACKNOWLEDGEMENTS 175 LIST OF PUBLICATIONS 179 VI List of Abbreviations ABL-ISDB - Antibiotic Literature In Dha - Dehydroalanine Silico Database DH Domain - Dehydratase Domain ACE - Angiotensin II Converting Enzyme DMSO - Dimethylsulfoxid ACP - Acyl Carrier Protein DNA - Deoxyribonucleic Acid A Domain - Adenylation Domain E Domain - Epimerase Domain antiSMASH - Antibiotics & ER Domain - Enoylreductase Secondary Metabolite Analysis Domain Shell ESI - Electrospray Ionization ARTS - Antibiotic Resistant Target GC Content - Guanine-Cytosine Seeker Content AT - Acyltransferase Domain GCF - Gene Cluster Family ATP - Adenosine Triphosphate GNPS - Global Natural Product BAGEL - Bayesian Analysis of Social Molecular Networking Gene Essentiality HMBC - Heteronuclear Multiple- BGC - Biosynthetic Gene Cluster Bond Correlation Spectroscopy BiG-SCAPE - Biosynthetic Gene HPLC - High Performance Liquid Similarity Clustering and Chromatography Prospecting Engine HSQC - Heteronuclear Single C Domain - Condensation Domain Quantum Coherence CDS - Coding DNA Sequences KEGG - Kyoto Encyclopedia of Genes and Genomes CFM - Competitive Fragmentation Modeling KS Domain - Ketosynthetase Domain CLUSEAN - Cluster Sequence Analyzer KR Domain - Keto-Reductase Domain COSY - Homonuclear Correlation Spectroscopy LC-MS - Liquid Chromatography - Mass Spectrometry Da - Dalton VII m/z - Mass-to-Charge Ratio O Domain - Oxidase Domain Mb - Megabases PCP - Peptide Carrier Protein MeCN - Acetonitrile PK - Polyketide MiBIG - Minimum Information about PKS - Polyketide Synthase a Biosynthetic Gene Cluster PRPS - Post-Ribosomal Peptide MS - Mass Spectrometry Synthesis MS2 - Tandem Mass Fragmentation R Domain - Reduction Domain MT Domain - Methyltransferase RBS - Ribosomal Binding Site Domain RiPP - Ribosomally Synthesized MUSCLE - Multiple Sequence and Post-Translationally Modified Comparison by Log- Expectation Peptide NMR - Nuclear Magnetic RNA - Ribonucleic Acid Resonance rRNA - Ribosomal RNA NOESY - Nuclear Overhauser Effect Spectroscopy TE Domain - Thioesterase Domain NP - Natural product TOCSY - Total Correlation Spectroscopy NRP - Non-Ribosomal Peptide tRNA - Transfer RNA NRPS - Non-Ribosomal Peptide- Synthetase tmRNA - Transfer-Messenger RNA UV - Ultraviolet VIII General Introduction 1 General Introduction 1 General Introduction any plants, fungi and bacteria are capable to produce specialized M metabolites (also known as natural products (NPs) or secondary metabolites). From a medicinal chemistry perspective, they are defined as low molecular weight (<3000 Da) organic molecules that usually have no primary role in the metabolism of the producing organism and do not immediately partake in processes essential for cell survival. [1-3] Many NPs can induce specific biological responses from organisms by selectively interacting with their cellular machinery. An example is nicotine, a NP most prominently occurring in the tobacco plant, which acts as a strong insecticide and protects plant leaves from insect infestation. [4] Still, in many cases, the ecological function of NPs is unclear. However, their cellular energy cost and elaborate structures suggest that they benefit the producing organism in some way and grant an evolutionary advantage. [3,5] Due to their diverse and potent bioactivities, many NPs or their derivatives have found their way into pharmacopoeias. Over the last four decades alone, 66% of approved small-molecule drugs were NPs or derivatives thereof (see Figure 1). They encompass antitumor drugs, antibiotics, immunosuppressants, analgesics and lipid-lowering agents, to name a few. In the field of antibacterial drugs, 71% of approved drugs are derived from microbial sources. [6] Fig. 1. Origin of small molecule drugs (1981-2019, n=1394). S: synthetic drug; S/NM: synthetic drug/mimic of NP; S*: synthetic drug with NP pharmacophore; S*/NM: synthetic drug with NP pharmacophore/NP mimic; N/NB: unaltered NP/botanical drug; ND: NP derivate. Adapted from Newman and Cragg, 2020. [6] 2 General Introduction Several thousand bioactive NPs were isolated from filamentous actinomycetes, prolific producers of various classes of metabolites. [1] Examples are the antibiotics streptomycin (1) from Streptomyces griseus [7,8] and vancomycin (2) from Amycolatopsis orientalis, [9,10] the anti-cancer drug daunorubicin (3) from Streptomyces peucetius, [11] the anti-fungal amphotericin B (4) from Streptomyces nodosus, [12] or the immunosuppressant rapamycin (5) from Streptomyces hygroscopicus (see Figure 2). [13-15] Despite the impressive track record of important drugs discovered from nature, large pharmaceutical companies have largely withdrawn from natural product research in the last decades. The loss in popularity of NPs has been explained in part by the supposedly higher productivity of large, synthetic combinatorial libraries. Further, high cost of structural elucidation and severe rediscovery rate of NPs in traditional
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