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Bisheriger Stand Des Wissens Genetische und biochemische Charakterisierung von Enzymen des anaeroben Monoterpen-Abbaus in Castellaniella defragrans Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften ― Dr. rer. nat. ― Dem Fachbereich Biologie/Chemie der Universität Bremen vorgelegt von Frauke Lüddeke Bremen, November 2011 Diese Arbeit wurde von Oktober 2008 bis November 2011 am Max-Planck-Institut für Marine Mikrobiologie in Bremen angefertigt. Teile dieser Arbeit sind bereits veröffentlicht oder zur Veröffentlichung eingereicht. Erster Gutachter: Prof. Dr. Friedrich Widdel Zweiter Gutachter: PD Dr. Jens Harder Tag des Promotionskolloquiums: 14.12.2011 Zusammenfassung III Zusammenfassung Das Betaproteobakterium Castellaniella (ex Alcaligenes) defragrans metabolisiert anaerob Monoterpene zu CO2 unter denitrifizierenden Bedingungen. Im Abbau involviert und initial charakterisiert sind eine Linalool Dehydratase-Isomerase (ldi/LDI) und eine Geraniol-Dehydrogenase (geoA/GeDH), während für eine Geranial-Dehydrogenase (geoB/GaDH) ein Kandidatengen gefunden wurde. In dieser Arbeit wurde ein genetisches System für C. defragrans basierend auf dem Suizid- Vektor pK19mobsacB entwickelt und Deletionsmutanten generiert. Die physiologische Charakterisierung bestätigte den postulierten Abbauweg für β-Myrcen in vivo und deckte die Existenz eines bislang unbekannten Monoterpen-Stoffwechselwegs sowie neue Enzymaktivitäten auf. Neben den genetischen Studien wurde die biochemische Charakterisierung der Enzymaktivitäten nach heterologer Überexpression in E. coli fortgesetzt. Die bifunktionale LDI katalysiert die Hydratisierung von β-Myrcen zu Linalool und die Isomerisierung zu Geraniol. Der enantiomere Überschuss dieser Reaktion lag bei 95.4 % für (S)-(+)-Linalool. Die Aktivität der LDI wurde durch chemische Modifikation von Cystein, Histidin, Asparagin- und Glutaminsäuren gehemmt. Die Deletion des ldi-Gens in C. defragrans bewirkte i) keinen Effekt auf den Abbau zyklischer Monoterpene, ii) ausbleibendes Wachstum auf β-Myrcen und iii) die Nutzung von (R,S)-(±)-Linalool als Kohlenstoffquelle. Die heterolog überexprimierte GeDH wurde homogen gereinigt. Nach nativer Polyacrylamidgelelektrophorese in Kombination mit einer Aktivitätsfärbung wies die GeDH ein natives Molekulargewicht (MG) von 85 kDa und damit eine Konformation als Dimer auf. Die Kinetik des rekombinanten Enzyms korreliert mit der Kinetik des aus C. defragrans gereinigten Enzyms. Die Affinität war für Geraniol im Vergleich mit Geraniol-Dehydrogenasen aus unterschiedlichen Organismen bemerkenswert hoch. Die Deletion des geoA-Gens verursachte ein verlangsamtes Wachstum auf Monoterpenen, was auf die Beteiligung weiterer Alkoholdehydrogenasen, welche die fehlende GeDH-Aktivität teilweise ausgleichen können, schließen lässt. Das Kandidatengen für eine durch Wachstum auf Monoterpenen induzierte Aldehyddehydrogenase vermittelte nach Expression in E. coli eine spezifische Geranial- Dehydrogenase-Aktivität im stöchiometrischen Verhältnis zu NAD+. Das cis-Isomer Neral wurde nicht umgesetzt. Die Dehydrogenasen sind die ersten molekular charakterisierten bakteriellen Dehydrogenasen mit Monoterpenoid-Spezifität. Abstract IV Abstract Castellaniella (ex Alcaligenes) defragrans is a betaproteobacterium metabolizing monoterpenes anaerobically under denitrifying conditions. Metabolite studies as well as a differential proteomic approach led to the identification of a linalool dehydratase- isomerase (ldi/LDI), a geraniol dehydrogenase (geoA/GeDH) and a candidate gene for a geranial dehydrogenase (geoB/GaDH). The LDI and GeDH were subjected to an initial biochemical characterization. In order to gain insight into the in vivo function of these genes a genetic system for C. defragrans was developed based on a suicide vector. After confirmation of the correct genetic background the physiological characterization of the obtained deletion mutants verified the postulated degradation pathway for β-myrcene. Besides, the results disclosed another monoterpene degradation pathway as well as novel enzyme activities. In addition to the genetic and physiological characterization the enzymes were heterologously expressed in E. coli and biochemically studied. The bifunctionally LDI catalyzes enantiospecifically the hydration of β-myrcene to (S)-(+)- linalool with an enantiomeric excess of > 95 % that is further isomerised to geraniol. Chemical modification of cysteine, histidine, aspartic and glutamic acid residues inhibited the enzyme activity. By the deletion of the ldi gene in C. defragrans a phenotype was caused that lost the ability of degrading the acyclic β-myrcene, but cyclic monoterpene degradation was not effected. A novel enzyme activity acting on (R,S)-(±)-linalool was observed, too. The heterologously expressed GeDH was purified to homogeneity and native PAGE in combination with an activity staining revealed the native conformation as dimer. With regards to their kinetic properties recombinant and wild type GeDH correlated well with a high affinity for geraniol. Due to the deletion of the geoA mutant strains revealed an impaired growth on monoterpenes suggesting the presence of further alcohol dehydrogenases acting on geraniol. The candidate gene for a geranial dehydrogenase, which was found to be induced by growth on monoterpenes, interceded specifically the oxidation of geranial. The cis-isomer was not converted. The formation of NAD+ was in a stoichiometric ratio. To our knowledge, both GeDH and GaDH are the first monoterpenoid specific dehydrogenases originating from a bacterium. Inhaltsverzeichnis III Inhaltsverzeichnis Abkürzungen V Teil I Einleitung 1 1. Isopren und Monoterpene 1 1.1. Grundstruktur und Biosynthese isoprenoider Naturstoffe 1 1.2. Ökologische und ökonomische Bedeutung von Terpenen und Monoterpenen 5 2. Biologischer Abbau von Kohlenwasserstoffen 9 2.1. Klassifizierung der Kohlenwasserstoffe 9 2.2. Mikrobielle Mechanismen zur Kohlenwasserstoffaktivierung 9 2.3. Aerober Abbau von Monoterpenen 12 2.4. Anaerober Abbau von Monoterpenen 15 3. Castellaniella defragrans Stamm 65Phen 17 4. Bakterielle genetische Systeme 20 5. Aufgabenstellung der Arbeit 24 Teil II Darstellung der Ergebnisse in Manuskripten 25 A. Liste der Manuskripte und Erläuterungen 25 B. Publikationen/ Manuskripte 28 1. Linalool dehydratase-isomerase, a bifunctional enzyme in the anaerobic degradation of monoterpenes 29 2. Enantiospecific (S)-(+)-linalool formation from β-myrcene by linalool dehydratase-isomerase 41 3. Short report: inhibition studies of the linalool dehydratase-isomerase activity with amino acid modifying reagents 46 4. Geraniol dehydrogenase and geranial dehydrogenase induced in the anaerobic monoterpene degradation of Castellaniella defragrans 50 Inhaltsverzeichnis IV 4.1. Additional information: geraniol dehydrogenase 70 4.1.1. Development of a purification protocol for the recombinant GeDH 70 4.1.2. Development of a geraniol dehydrogenase activity staining 71 4.1.3. pH optimum 72 5. A genetic system for Castellaniella defragrans 65Phen demonstrates the physiological role of a high-affinity geraniol dehydrogenase 73 6. Genetic evidence for a second anaerobic monoterpene-activating enzyme in Castellaniella defragrans 103 Teil III Gesamtübergreifende Diskussion und Ausblick 125 1. Genetische Manipulierbarkeit von C. defragrans 125 2. Der anaerobe Abbau von β-Myrcen in C. defragrans 128 2.1. Bioverfügbarkeit der Kohlenstoffquelle 128 2.2. Linalool Dehydratase-Isomerase 129 2.2.1. (R,S)-(±)-Linalool umsetzende Enzymaktivität 132 2.3. Geraniol-Dehydrogenase 133 2.4. Geranial-Dehydrogenase 135 3. Physiologie des Monoterpen-Abbaus in C. defragrans 135 4. Biotechnologische Anwendungsaspekte für Enzyme des Monoterpen-Abbaus aus C. defragrans 137 Referenzen 141 Danksagung VII Abkürzungen V Abkürzungen ADH Alkoholdehydrogenase AlDH Aldehyddehydrogenase atu azyklische Terpennutzung/ acyclic terpene utilization CFU Kolonie-bildende Einheit/ colony forming units CMC 1-Cyclohexyl-N-(2-morpholinoethyl)carbodiimid Cre verursacht Rekombination/ causes recombination CV Säulenvolumen/ column volume DEPC Diethylpyrocarbonat DH Dehydrogenase DIFP Diisopropylfluorophosphat DMAPP Dimethylallylpyrophosphat DTT Dithiothreitol DXP 1-Deoxy-D-xylulose-5-phosphat EDTA Ethylendiamintetraessigsäure Flp Flippase FPP Farnesylpyrophosphat FRT Flippase Zielsequenz für Rekombination/ Flippase recombination target geoB/GaDH Geranial-Dehydrogenase (Gen/Protein) GC Gaschromatographie/-y geoA/GeDH Geraniol-Dehydrogenase (Gen/Protein) GGPP Geranylgeranylpyrophosphat GI Geraniol-Isomerase GPP Geranylpyrophosphat GRAS generally recognized as safe HMN 2,2,4,4,6,8,8-Heptamethylnonan IAA Iodessigsäure/ iodo acetic acid i. d. Innendurchmesser/ inner diameter IPP Isopent-3-enylpyrophosphat IPTG Isopropyl-ß-D-thiogalactopyranosid LC Flüssigchromatographie/ liquid chromatography Abkürzungen VI LDH Linalool-Dehydratase ldi/LDI Linalool Dehydratase-Isomerase (Gen/Protein) MDR medium-chain dehydrogenase/reductase MEP 2C-Methyl-D-erythritol-4-phosphat MoCo Molybdän-Kofaktor MVA Mevalonat NBT Nitroblautetrazoliumchlorid/ nitroblue tetrazolium chloride NEM N-Ethylmaleimid OPP Pyrophosphat ORF offener Leserahmen/ open reading frame PAGE Polyacrylamidgelelektrophorese PCR Polymerasekettenreaktion/ polymerase chain reaction PES Phenazinethosulfat PMSF Phenylmethylsulfonylfluorid SDS Sodiumdodecylsulfat Einleitung 1 Teil I Einleitung 1. Isopren und Monoterpene 1.1. Grundstruktur und Biosynthese isoprenoider Naturstoffe Der Begriff Terpen beschreibt eine heterogene
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