Multi-enzyme in vitro systems for biocatalysis: Concepts, optimization and application

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1 DISS. ETH NO Multi-enzyme in vitro systems for biocatalysis: Concepts, optimization and application A dissertation submitted to ETH ZURICH for the degree of Doctor of Sciences presented by Matthias Bujara Dipl. Biotechnol., TU Braunschweig born citizen of Germany accepted on the recommendation of: Prof. Dr. Sven Panke (ETH Zurich, Switzerland), examiner Prof. Dr. Uwe Sauer (ETH Zurich, Switzerland), co-examiner Prof. Dr. Ralf Takors (University Stuttgart, Germany), co-examiner 2011

2 Abstract The enantio- and regioselectivity of enzymes and their ability to operate under a common set of environmental conditions makes them excellent catalysts for complex organic syntheses, for example for the production of pharmaceutically important and multifunctional sugar and sugar-like molecules. Mimicking nature by combining several enzymes to multi-enzyme reactions has the potential to convert cheap substrates such as glucose to valuable products in a one-pot reaction. This thesis addresses conceptual and practical issues with regard to making multi-enzyme systems available for complex synthesis tasks. On the practical side, it opens an alternative route for dihydroxyacetone phosphate (DHAP) production starting from glucose in order to use DHAP for aldolase-catalyzed synthesis of unnatural monosaccharides. On the conceptual side, it suggests new routes and methods for recruiting and optimizing multienzyme systems from a single cultivation. The cofactor-neutral conversion of glucose to DHAP requires a ten-enzyme system. DHAP is a versatile building block for the aldolase-catalyzed synthesis of unnatural monosaccharides, which acts as a donor for a set of four different DHAP-dependent aldolases, each realizing a different stereochemistry for the resulting vicinal diols. These aldolases accept a broad variety of aldehydes but strictly require DHAP as the donor substrate. DHAP is formed as a regular intermediate in standard glycolysis from cheap glucose, opening in principle the route to simple and cheap manufacturing. Accumulation of DHAP in batch reactions using glucose as substrate and cell free extract from a strain carrying a triosephosphate isomerase (tpia) deletion demonstrated the principle functionality of recruiting multi-enzyme systems from crude cell extracts, but also indicated the requirement to remove side reactions which are also part of the complex cell free extract. DHAP production from adenosine nucleotides added as cofactors was identified as an important side reaction and removed by deleting the gene for AMP nucleosidase. After adapting the topology of the enzyme network, a next step was the optimization of the system composition. In contrast to mono-enzyme biotransformations, an improved DHAP production is here the result of optimizing the performance of at least 10 constituent enzymes, involving at least 16 different compounds. To circumvent the laborious analysis of multiple samples by time consuming methods such as combinations of chromatography and mass spectrometry, a metabolomic real-time analysis tool was developed, which continuously injected the reactor effluent into a mass spectrometer and thus allowed the comprehensive and quantitatively accurate, real-time analysis of the in vitro reaction network. This setup was used to optimize the in vitro production of DHAP based on E. coli s glycolysis. A concerted bottleneck in the glucokinase reaction (1 st reaction in the cascade) and the fructosebisphosphate aldolase reaction (4 th reaction in the cascade) was identified, which could be I

3 removed by adding purified enzyme preparations. Using this information as a blueprint, a synthetic four-gene operon was constructed which produced DHAP as efficiently as predicted. The system for improved DHAP production was then exploited for the synthesis of unnatural monosaccharides. An additional aldolase was encoded in the operon as a fifth gene, since the endogenous E. coli aldolase does not accept aldehydes other than glyceraldhyde-3-phosphate, thus contributing to the selectivity of the system. Metabolic real-time analysis guided two optimization rounds for the construction of a five-gene operon including the gene for the Staphylococcus carnosus FruA aldolase. Next, frua was substituted by genes encoding aldolases which catalyze a stereochemically different aldol reaction and the functionality of these aldolases was verified by metabolic real-time analysis and HPLC-MS. Cell free extract from a strain carrying the five-gene operon with S. carnosus frua was finally used in fed-batch reactions for the preparative synthesis of different unnatural monosaccharides yielding product concentrations above 50 mm. The production of pharmaceutically relevant iminocylitols for the use as precursors for glucosidase inhibitors could thus be demonstrated as well. In a further step to improve our understanding of the complexities of a cell free extract-derived biocatalytic system, we implemented a bioinformatics tool to analyze the topological complexity of the system in which the desired pathway is embedded. As the unwanted conversion of adenosine phosphates to DHAP illustrates, cell-free extract-based biocatalytic systems are usually embedded in metabolic networks, which makes chemical insulation of the production system necessary. For a more systematic assessment of potentially disturbing reactions an analysis tool for network topology in cell free systems was implemented based on genome scale metabolic models, for which proper constraints were identified to reflect the in vitro situation. As a positive control of the tool, it correctly suggested the interfering formation of DHAP from adenosine nucleotides. II

4 Zusammenfassung Enzyme sind durch ihre Enatio- und Regioselektivität vielversprechende Katalysatoren für die Synthese von komplexen organischen Molekülen, wie z.b. pharmazeutisch wichtigen Zucker oder Zucker-ähnlichen Substanzen. Durch die Kombination verschiedener Enzyme lässt sich die Natur imitieren, indem einfache Substrate wie Glukose in einem einzigen Reaktionsraum in wertvolle Metaboliten umgewandelt werden. In dieser Arbeit werden Konzepte und praktische Aspekte der Multi-Enzym Katalyse behandelt. Die Anwendung eines alternativen Wegs für die Produktion von Dihydroxyacetonphosphat ausgehend von Glukose wird aufgezeigt und Konzepte für die Herstellung und Optimierung von Multi-Enzym Systemen aus einer einzelnen Kultivierung werden entwickelt. Fundamentale Fragen der Multi-Enzym Katalyse für die Feinchemie wurden anhand des glykolytischen Netzwerks von E. coli, das zur Produktion von DHAP herangezogen wurde, behandelt. DHAP ist ein essentieller Baustein für die Synthese von nicht-natürlichen Monosachariden mittels DHAP-abhängiger Aldolasen. Es gibt vier verschiedene Aldolasen, welche vier stereochemisch unterschiedliche Kohlenstoff-Kohlenstoff Bindungen zwischen dem essentiellen Donor-Molekül DHAP und einem (nahezu beliebigen) Aldehyd knüpfen. DHAP ist ein natürliches Intermediat der Glykolyse und kann daher ausgehend von preiswerter Glukose hergestellt werden. Die prinzipielle Funktionalität dieses Ansatzes wurde durch die Produktion von DHAP in Batch-Reaktionen mit zellfreiem Extrakt von einer E. coli triosephosphat-isomerase (tpia) Knockoutmutante gezeigt. Das Problem der Reaktionskomplexität in zellfreiem Extrakt wurde anhand der Produktion von DHAP aus ATP deutlich und konnte durch einen zusätzlichen Knockout beseitigt werden. Als nächstes wurde das Reaktionssystem optimiert. Eine Voraussetzung hierfür ist eine vollständige und exakte Charakterisierung des Systems, da nur so potentielle Limitationen schnell gefunden werden können. Die zeitaufwendige Analyse von vielen Proben durch eine Kombination aus Chromatographie und Massenspektrometrie wurde durch die Entwicklung eines metabolischen Echtzeit Messsystems beschleunigt. Das Messsystem injiziert den Reaktorausfluss kontinuierlich in ein Massenspektrometer wodurch ein vollständiger, quantitativer Datensatz in Echtzeit aufgenommen werden kann. Diese Methode wurde für die in vitro Optimierung der zellfreien E. coli Glykolyse verwendet. Durch Zugabe gereinigter Enzyme wurde eine Limitation durch die Glucokinase und Fructosebisphosphat-Aldolase im Reaktionssystem identifiziert die nur durch eine erhöhte Aktivität beider Enzyme kompensiert werden konnte und dadurch die stationäre DHAP Konzentration um das 2.5-fache erhöhte. Diese Informationen wurden für die Konstruktion eines Operons verwendet, das die Expression und somit die Aktivität dieser Enzyme in der lebenden Zelle erhöht. Ein synthetisches 4-Gen Operon steigerte letztendlich die DHAP-Produktion um das 2.5-fache ohne dass zusätzlich gereinigtes Enzym zugegeben werden musste. III

5 Zur Erweiterung des DHAP-Produktionssystem für die Synthese von unnatürlichen Monosachariden musste ein fünftes Gen in das Operon integriert werden, da die endogene E. coli Fructosebisphosphat-Aldolase nur Glyzerin-3-phosphat als Aldehyd akzeptiert. Ein 5-Gen Operon mit der Staphylococcus carnosus FruA Aldolase für die synthetische Aldolase Reaktion wurde konstruiert und die Fuktionalität wurde durch metabolischer Echtzeit Analyse funktional bestätigt. Anschliessend wurde die S. carnosus FruA Aldolase durch andere Aldolasen ersetzt, die eine Kohlenstoff-Kohlenstoff Bindung mit einer anderen Stereochemie katalysieren. Zellfreies Extrakt von einem Stamm mit 5-Gen Operon wurde für die unnatürliche Monosacharid Produktion in Batch-Reaktionen verwendet. Damit wurden Produktkonzentrationen von mehr als 50 mm erreicht. Darüber hinaus konnten pharmazeutisch relevante Iminocylitol-Vorstufen synthetisiert werden, die Anwendung als Glucosidase-Inhibitoren finden. Katalytische Multi-Enzym Systeme, basierend auf zellfreiem Extrakt, sind in der Regel Bestandteil eines größeren metabolischen Netzwerks, was unweigerlich zu ungewollten Nebenreaktionen führen kann, wie am Beispiel der DHAP Produktion aus ATP gezeigt wurde. Für die systematische Suche nach potentiell störenden Reaktionen wurde eine computerbasierte Analyse der Netzwerktopologie initiiert, die auf stöchiometrischen Genomweiten metabolischen Modellen basiert. Metabolische Modelle konnten für die Analyse von zellfreien Systeme adaptiert werden indem Randbedingungen geändert und neue Randbedingungen eingeführt wurden. Dadurch war es z.b. möglich den Reaktionspfad von ATP zum DHAP vorherzusagen. IV

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