THE SPATIOTEMPORAL REGULATION AND MECHANISM OF ACTION OF FUNGAL NEMATOTOXIC DEFENSE EFFECTORS
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1 DISS. ETH NO THE SPATIOTEMPORAL REGULATION AND MECHANISM OF ACTION OF FUNGAL NEMATOTOXIC DEFENSE EFFECTORS A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) presented by STEFANIE SOFIA SCHMIEDER Dipl. Biol., Universtität Tübingen born on citizen of the Federal Republic Germany accepted on the recommendation of Prof. Dr. Markus Aebi Dr. Markus Künzler Prof. Dr. Julia Vorholt Prof. Dr. Han Wösten Prof. Dr. Els van Damme 2015
2 Summary Summary Their saprotrophic life-style and growth as a filamentous network make fungi frequent prey for the meso- and microfauna inhabiting the soil. One of the most abundant phyla within the soil microfauna are nematodes and the phylum includes many fungivorous species. To defend themselves against predation by nematodes, fungi employ a protein effector-based defense. This thesis explores the spatiotemporal regulation of a protein effector-based defense in Coprinopsis cinerea against the mycophagous nematode Aphelenchus avenae. Chapter 1 provides a comprehensive overview of the biophysical properties of fungal networks, the establishment of such networks and the biological and ecological consequences of filamentous fungal growth. The chapter will give insight into the mechanism governing growth and translocation of nutrients within the network. It summarizes our current knowledge on protein-based fungal defense strategies with focus on holo- and chimerolectins and their similarity to classical bacterial or plant AB-toxins. Finally, the receptor and endocytic trafficking requirements of AB-toxins are discussed. In chapter 2, the interaction between the basidiomycete C. cinerea and the mycophagous nematode A. avenae is discussed. Tailor-made microfluidic platforms were designed to monitor this interaction in real time and at single hypha resolution. The choice of an open microfluidic system allowed for precise extraction of mycelial material for further characterization of the protein-based anti-nematode defense of C. cinerea. Moreover, we propose a novel pathway for inter-mycelial long-distance communication via specialized, differentiated hyphae in the vegetative mycelium of C. cinerea. These hyphae not only allow the long distance transmission of fungal defense but also serve as routes for the transport of solutes and nutrients. Chapter 3 comprises the biochemical and molecular characterization of a new class of fungal defense effector proteins exemplarily on the chimerolectin CCTX2. The specific upregulation of CCTX2 and its paralog CCTX1 within vegetative hyphae of C. cinerea upon predation, as well as its toxicity towards the model organism Caenorhabditis elegans highlights their involvement in fungal defense. We use C. elegans to dissect the molecular basis of its toxicity. The receptor requirements on 7
3 Summary the target host cells, as well as the endocytic trafficking pathways exploited by this family of proteins show striking similarity to bacterial and plant AB-toxins. We propose therefore that this class of defense and effector proteins is not limited to the bacterial and plant kingdoms but is also employed within the fungal kingdom as a defense strategy. In Chapter 4 a novel heterologous system for the expression of putative defense proteins is presented. We used Ashbya gossypii, a filamentous yeast as expression host for fruiting body lectins and other cytoplasmic fruiting body proteins to study their toxicity against the obligate mycophagous nematode A. avenae. The lack of defense proteins in A. gossypii offered the advantage of individually testing putative toxic proteins against fungivores. The results indicate a narrower susceptibility profile in fungivorous nematodes compared to the bacteriovore C. elegans; with the latter being commonly used to test potential novel nematotoxic protein candidates. These differences in susceptibility of different nematode species indicate a potential co-evolution between predator and prey. Finally, chapter 5 presents the conclusions of this thesis and gives an outlook for strategies to further investigate protein-based defense in fungi. 8
4 Zusammenfassung Zusammenfassung Das filamentöse und großflächige Wachstum vieler Pilze, sowie deren Organisation als vernetztes Myzel, stellt im Boden eine erhebliche Herausforderung an den Organismus dar. Kontakt mit potentiellen Frassfeinden der Makro- sowie Mikrofauna beispielsweise, ist unvermeidbar. Zur Pilz-fressenden Mikrofauna zählen Nematoden, eine der artenreichsten Gruppen im Tierreich. Die vorliegende Doktorarbeit untersucht den Zusammenhang eines Protein-basierten Abwehrmechanismus im Myzel des Basidiomyceten Coprinopsis cinerea gegen den obligat Pilz-fressenden Nematoden Aphelenchus avenae. Dabei wird speziell die Regulation einiger Abwehrproteine, sowie deren Ausbreitung innerhalb des Myzels untersucht. Kapitel 1 gibt einen Literaturüberblick zum Thema pilzliches Wachstum, die zugrunde liegenden biophysikalischen Eigenschaften der Hyphe, sowie die Entwicklung des Myzels in ein Netzwerk bestehend aus einzelnen Hyphen. Diese spezielle Wachstumsform hat Auswirkungen auf die Physiologie des Organismus, da die Aufnahme unterschiedlicher Nährstoffe beispielsweise unabhängig voneinander sein kann. Dies setzt jedoch ein Transportsystem voraus, das für den Austausch und die Verteilung von Nährstoffen verantwortlich ist. Des Weiteren werden Holo- und Chimärolektine besprochen. Eine Proteingruppe, die in Zusammenhang mit der Protein-basierten Abwehr in C. cinerea steht. Chimärolektine weisen eine gewisse Ähnlichkeit zu bakteriellen oder pflanzlichen AB- Toxinen auf, weshalb zusätzlich der Toxizitätsmechanismus letzterer beschrieben wird. In Kapitel 2 wird die Interaktion zwischen C. cinerea und dem pilz-fressenden Nematoden A. avenae charakterisiert. Diese ist sehr dynamisch und erfordert die Verwendung spezieller Mikrofluidik Chips, die zeitnahe Beobachtung auf dem Niveau einzelner Hyphen zulässt. Der offene Charakter des Chips ermöglichte zusätzlich das Extrahieren pilzlichen Materials zur weiteren Analyse, um neue potentielle Abwehrproteine zu bestimmen. 9
5 Zusammenfassung Die detaillierte Analyse der Abwehrreaktion in C. cinerea weisst auf ein spezielles Transportsystem innerhalb des Myzels hin. Dieses erlaubt das Austauschen von Information über größere Distanz, auch in Bereiche des Myzels, die nicht in direktem Kontakt zu beispielsweise, den Nematoden standen. Des Weiteren ermöglicht dieses System den Transport und Austausch von Nährstoffen. Kapitel 3 umfasst die biochemische und molekularbiologische Charakterisierung einer neuen Gruppe von Abwehrproteinen, die in C. cinerea gefunden wurden. In C. cinerea wird diese Proteinklasse speziell durch Nematoden induziert. Am Beispiel von CCTX2 wird im Modelorganismus C. elegans die Wirkungsweise dieser Proteinklasse gezeigt. Der Rezeptor des Proteins auf der Zielzelle, der Toxizitätsmechanismus, sowie der interzelluläre Endocytoseweg konnten entschlüsselt werden. Die Ähnlichkeit zu bakteriellen und pflanzlichen AB-Toxinen wird aufgewiesen und legt nahe, dass auch in Pilzreich solche Toxine zur Abwehr gegenüber Frassfeinden verwendet werden. In Kapitel 4 wird eine neue Methode zur Expression möglicher Abwehrproteine vorgestellt. Die Verwendung der filamentösen Hefe Ashbya gossypii zur Expression von Fruchtkörperproteinen erlaubt das Testen auf deren Toxizität gegenüber obligat Pilz-fressenden Organismen wie A. avenae. Da A. gossypii keine solchen Abwehrproteine besitzt, können einzelne potenziell toxische Proteine getestet werden. Die partielle Resistenz A. avenaes auf manche Abwehrproteine, die mit Hilfe dieser Methode gefunden wurden, spricht für eine evolutionäre Anpassung Pilzfressender Nematoden gegenüber Bakterien-fressenden Nematoden wie C. elegans, der grundsätzlich sensitiv gegenüber solchen Proteinen ist. 10
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