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Exploiting Gene Regulation As an Approach to Identify, Analyze And Exploiting gene regulation as an approach to identify, analyze and utilize the biosynthetic pathways of the glycopeptide ristomycin A and the zincophore [S,S]-EDDS in Amycolatopsis japonicum DISSERTATION der Mathematisch-Naturwissenschaftlichen Fakultät der Eberhard Karls Universität Tübingen zur Erlangung des Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) vorgelegt von Marius Steffen Spohn aus Tettnang Tübingen 2015 Exploiting gene regulation as an approach to identify, analyze and utilize the biosynthetic pathways of the glycopeptide ristomycin A and the zincophore [S,S]-EDDS in Amycolatopsis japonicum DISSERTATION der Mathematisch-Naturwissenschaftlichen Fakultät der Eberhard Karls Universität Tübingen zur Erlangung des Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) vorgelegt von Marius Steffen Spohn aus Tettnang Tübingen 2015 Erklärung Ich erkläre hiermit, dass ich die zur Promotion eingereichte Arbeit selbständig verfasst, nur die angegebenen Quellen und Hilfsmittel benutzt und Stellen, die wörtlich oder inhaltlich nach den Werken anderer Autoren entnommen sind, als solche gekennzeichnet habe. Eine detaillierte Abgrenzung meiner eigenen Leistungen von den Beiträgen meiner Kooperationspartner habe Tag der mündlichen Qualifikation: 27.01.2016 ich im Anhang vorgenommen. Dekan: Prof. Dr. Wolfgang Rosenstiel 1. Berichterstatter: PD Dr. Evi Stegmann . 2. Berichterstatter: Prof. Dr. Karl Forchhammer Unterschrift 3. Berichterstatter: Prof. Dr. Christian Hertweck Tübingen, den 30.11.2015 Table of content Table of content Table of content Table of content Table of content 2.2 Identification of the [S,S]-EDDS biosynthetic genes by exploiting knowledge of zinc Zusammenfassung i dependent transcriptional regulation 16 Abstract iii 2.2.1 The zinc responsive zinc uptake regulator Zur controls the [S,S]-EDDS List of publications v biosynthesis 16 Contributions vi 2.2.2 Zur controls the high affinity zinc uptake system ZnuABC 17 Abbreviations vii 2.2.3 The rational screening of the A. japonicum Zur regulon revealed putative [S,S]- EDDS biosynthetic genes 17 1. Introduction 1 2.2.4 The transcription of the aesA-D operon is zinc responsively regulated by Zur 18 1.1 The genus Amycolatopsis: a valuable source of secondary metabolites 1 2.2.5 The aes genes are essential for [S,S]-EDDS production 19 1.2 Glycopeptide antibiotics 2 2.2.6 The [S,S]-EDDS biosynthesis as response to zinc deficiency is phylogenetically 1.2.1 Structural categorization of glycopeptides 3 clustered 19 1.2.2 Glycopeptide antibiotics biosynthesis: precursor supply 3 1.2.3 Glycopeptide antibiotics biosynthesis: assembly of the heptapeptide 4 3. Discussion 21 1.2.4 Glycopeptide antibiotics biosynthesis: modification of the heptapeptide 5 3.1 A. japonicum genome contains a silent gene cluster directing the biosynthesis of 1.2.5 Transcriptional regulation of glycopeptide biosynthesis 5 ristomycin A 21 1.3 Ionophores: naturally occurring chelating agents 6 3.2 The [S,S]-EDDS biosynthetic genes were identified by a novel approach exploiting 1.3.1 Siderophore biosynthesis 6 knowledge in the field of zinc responsive gene regulation 25 1.3.2 Metal responsive regulation of ionophore biosynthesis 6 3.2.1 [S,S]-EDDS exemplifies the rare functionally class of zinc responsive ionophores 25 1.3.2.1 The ferric uptake regulator (Fur) 7 3.2.2 Elucidation of the Zur mediated zinc regulation enabled the identification of the 1.3.2.2 The iron dependent DtxR protein family 7 [S,S]-EDDS biosynthetic genes 28 1.3.2.3 The zinc uptake regulator (Zur) 8 3.2.3 The biogenesis of [S,S]-EDDS 30 1.4 Ethylenediamine-disuccinate (EDDS) 8 3.2.4 Biotechnological [S,S]-EDDS production 31 1.5 Genome mining: an empirical strategy to discover new natural products 9 1.6 Aim of the work 12 4. References 33 2. Results 13 5. Publications 43 2.1 Activation of a silent glycopeptide gene cluster in A. japonicum 13 5.1 Publication 1 43 2.1.1 A. japonicum encodes a silent glycopeptide gene cluster 13 5.2 Publication 2 81 2.1.2 Genome sequencing and Genome mining revealed a glycopeptide gene cluster 13 5.3 Publication 3 84 2.1.3 The cluster encoded transcriptional activator AjrR is functional 14 2.1.4 Structure elucidation revealed ristomycin A as product of A. japonicum 15 2.1.5 A. japonicum ristomycin A induces in vitro platelet aggregation 15 Zusammenfassung Zusammenfassung Zusammenfassung usammenassung Zusammenfassung einen Zink-sensitiven Regulator gewhrleistet wird. Die akterielle ink-Homöostase wird meistens durch den globalen Zink-speziische ranskriptionsregulator ur reguliert as ur Protein von A. Der mikrobielle Sekundärmetabolismus ist eine reichhaltige Quelle für Naturstoffe, von denen viele japonicum wurde identiiziert und detailliert charakterisiert Es konnten gezeigt werden, dass urAj klinische beziehungsweise industrielle Anwendung gefunden haben. Die Gattung Amycolatopsis ist die ranskription des hoch ainen inkaunahmesystems nuACAj durch seine ink-ahängige für die Synthese vieler Naturstoffe bekannt. Beispielsweise werden viele Glykopeptid-Antibiotika, wie indung an speziische NA indesequenzen reguliert Diese Zur-indesequenzen wurden das klinisch relevante Vancomycin oder das Balhimycin, von Stämmen dieser Gattung produziert. Im verwendet, um das A. japonicum Genom nach weiteren, urAj regulierten, Genen zu durchsuchen Gegensatz dazu wurde der Stamm Amycolatopsis japonicum nie als Produzent einer biologisch Dies führte zur Auindung des aesA-D perons. mangreiche ranskriptions-ntersuchungen aktiven Substanz beschrieben. Dieser Stamm produziert jedoch unter Zinkmangelbedingungen das ergaben, dass aesA-D Zink-ahängig von urAj reguliert wird Die eteiligung von aesA-D an der [S,S]- EDTA-Isomer Ethylendiamindisuccinat ([S,S]-EDDS). Diese zinkabhängige [S,S]-EDDS Produktion lässt EDDS konnte durch naktivierungsversuche nachgewiesen werden ustzlich hrte die eletion des darauf schließen, dass [S,S]-EDDS ein Zinkophor ist, das an der Zinkaufnahme beteiligt ist. inkregulators urAj (A. japonicum Δzur) dazu, dass auch in Gegenwart von hohen ink- [S,S]-EDDS weist Komplexbildungseigenschaften auf, die mit denen von EDTA vergleichbar sind. Im onzentrationen [S,S]-EDDS in hohen Mengen produziert wird. Gegensatz zu EDTA ist [S,S]-EDDS jedoch biologisch abbaubar. Die weitverbreitete industrielle A. japonicum Δzur ist eine erolgversprechende Ausgangsasis, um einen nachhaltigen und Anwendung von EDTA in Kombination mit dessen Unzugänglichkeit für biologische Abbauprozesse wirtschatlich verwertaren [S,S]-EDD Produktionsprozess zu entwickeln, der keiner imitierung führt zu einer umweltgefährdenden EDTA-Persistenz in aquatischen Lebensräumen. Der Naturstoff durch negative inlüsse von ink unterliegt [S,S]-EDDS ist deshalb ein nachhaltiger EDTA Ersatz mit einem verbesserten ökologischen Die trategie, ein vorhergesagtes, stilles Gencluster durch die xpression eines speziischen Fingerabdruck. egulators zu aktivieren, sowie auch die trategie, neue iosynthese-Gene durch die In dieser Arbeit wurden zwei molekulargenetische Strategien entwickelt, um die Biosynthese des harakterisierung eines globalen egulators, der speziische mweltsignale wahrnimmt, zu Glykopeptid-Antibiotikums Ristomycin A zu aktivieren und um die [S,S]-EDDS-Biosynthese-Gene in identiizieren, ermöglichte die harakterisierung neuer aturstosynthesewege in A. japonicum A. japonicum zu identifizieren. eide Anstze nutzen Erkenntnisse über regulatorische echanismen und esitzen das otenzial Untersuchungen des genetischen Potenzials der Gattung Amycolatopsis ließen vermuten, dass auch zukntig angewendet zu werden, um neue aturstoffe und neue ynthesewege zu identiizieren A. japonicum die Fähigkeit besitzt, ein Glykopeptid-Antibiotikum zu synthetisieren. Um dieses nicht exprimierte, sogenannte „stille Gencluster“ zu aktivieren, wurde ein molekulargenetischer Ansatz verwendet, bei dem der Biosynthese-spezifische Aktivator Bbr heterolog in A. japonicum exprimiert wurde. Bbr reguliert die Balhimycin-Biosynthese in Amycolatopsis balhimycina. In A. japonicum induzierte dessen Expression die Produktion von Ristomycin A, was durch HPLC-DAD, MS, MS/MS, HR-MS, und NMR-Analysen bestätigt werden konnte. Ristomycin A ist ein vielfach glykosyliertes Heptapeptid, das als Hauptwirkstoff in Diagnoseverfahren zur Bestimmung von angeborenen und weitverbreiteten Blutgerinnungsstörungen verwendet wird. Die Sequenzierung des A. japonicum Genoms und dessen computergestützte Auswertung führten zur Identifizierung des Biosynthese- Genclusters, das für die Synthese von Ristomycin A verantwortlich ist. Solche computergestützten Genomanalysen mittels verschiedenster bioinformatischen Plattformen werden heutzutage standardmäßig zur Identifizierung von Sekundärmetabolit-Gencluster angewandt, die bekannten Synthesemechanismen zugeordnet werden können. Allerdings konnten die [S,S]-EDDS-Biosynthese-Gene mit diesen Tools nicht entdeckt werden, was auf einen bislang nicht bekannten Biosynthesemechanismus hindeutet. Um diesen zu identifizieren, wurde ein neuer Ansatz entwickelt, der auf der Annahme beruht, dass die Zink-reprimierte [S,S]-EDDS-Biosynthese durch i ii i ii Abstract Abstract Astract Astract Abstract the identiication of the operon aesA-D. Extensive transcriptional analses and and shit assays aesA-D S,S he microbial secondar metaolism is a rich source for valuale products that have found their wa revealed that is zinc responsively regulated by ur and involved in [ ]-EDD iosynthesis, as S,S into various clinical and industrial applications A particularl productive bacterial
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