Research Collection. Doctoral Thesis. ETH Library. Author(s): Stöckli, Martina Angela. Publication Date: 2016
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1 Research Collection Doctoral Thesis Investigations on antagonistic bacterial-fungal interactions - analysis of molecules at the interface of the basidiomycete Coprinopsis cinerea with antagonistic bacteria Author(s): Stöckli, Martina Angela Publication Date: 2016 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 DISS. ETH NO Investigations on antagonistic bacterial-fungal interactions Analysis of molecules at the interface of the basidiomycete Coprinopsis cinerea with antagonistic bacteria A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) presented by Martina Angela Stöckli MSc ETH Biology born on citizen of Menznau, Luzern accepted on the recommendation of Prof. Dr. Markus Aebi Dr. Markus Künzler PD Dr. Pauli Kallio Prof. Dr. Bruce McDonald Prof. Dr. Leo Eberl 2016
3 Summary The dung-inhabiting basidiomycete Coprinopsis cinerea and its antagonistic interactions with bacteria, in particular on a cellular and molecular level was the subject of this PhD thesis. The first chapter gives an introduction into fungal ecology, bacterial-fungal interactions and fungal defense against bacteria. The focus lies on two different mechanisms of defense, constitutive and induced chemical defense and their effector molecules. The second chapter describes the development of a method to study bacterial-fungal interactions on a cellular level and over time using microfluidic devices. Two different devices were developed, one allowed to study the long term interactions of the two organisms and the other to exchange the fluid around fungal hyphae in a rapid manner. These tools gave an insight into the dynamic interaction between C. cinerea and the Gram-positive bacterium Bacillus subtilis. These bacteria attached in an end-on manner to only certain hyphae and exerted antifungal activity on single hyphae. The third chapter describes the identification and biochemical characterization of two paralogous intracellular fungal proteins. These proteins showed hydrolyzing activity towards N- acyl-homoserine lactones, quorum sensing molecules used by Gram-negative bacteria. C. cinerea hyphae acted as a sink for the quorum sensing molecules. The two fungal proteins showed homology to known bacterial lactonases. The occurrence of lactonase genes in basidiomycete genomes was correlated to the lifestyle of these fungi. The fourth chapter describes comparative transcriptomics of the C. cinerea vegetative mycelium challenged with either the Gram-positive bacterium B. subtilis or the Gram-negative bacterium Escherichia coli. C. cinerea responded to both bacterial species with the induction of a conserved gene set where genes coding for secreted proteins were overrepresented. The production of some of the induced gene products were confirmed in the bacteria-induced secretome by shotgun proteomics. A family of lysozyme and defensin-like proteins and their antibacterial activity against Gram-positive bacteria was more closely investigated. The fifth chapter characterizes one of the bacteria-induced genes identified in chapter four. Its gene product was confirmed to be involved in the biosynthesis of an antimicrobial secondary metabolite, lagopodin B. Lagopodin B was produced in response to co-cultivation of C. cinerea with bacteria or their cell-free supernatant. C. cinerea responded with induction of these genes in presence of both, Gram-negative bacteria and Gram-positive bacteria, even though the secondary metabolite exhibited inhibitory activity only towards Gram-positive bacteria. By using microfluidic devices, described in chapter two, and a promoter-reporter fusion construct the localization of gene induction was studied on cellular level. The sixth chapter gives a conclusion and an outlook for future research in fungal defense against bacterial antagonists. i
4 Zusammenfassung Diese Doktorarbeit befasst sich mit dem Dung bewohnenden Ständerpilz, dem struppigen Misttintling, Coprinopsis cinerea, und seinen antagonistischen Interaktionen mit Bakterien auf zellulärer und molekularer Ebene. Das erste Kapitel gibt eine Einleitung in die Ökologie der Pilze, Pilz Bakterien Interaktionen und der pilzlichen Abwehr gegen Antagonisten. Der Fokus liegt dabei auf Mechanismen der konstitutiv aktiven Abwehr und der induzierten Abwehr und den beteiligten Effektormolekülen. Das zweite Kapitel beschreibt die Entwicklung einer Methode, um Pilz-Bakterien Interaktionen auf zellulärer Ebene und über längere Zeit mit Hilfe von mikrofluidischen Plattformen zu untersuchen. Zwei verschiedene Plattformen wurden entwickelt, die eine, um die Interaktion zwischen Pilzhyphen und Bakterien über einen längeren Zeitraum zu untersuchen und die zweite, um das Medium, das die Hyphen umgibt, schnell auszutauschen. Mit Hilfe dieser Methode konnten neue Erkenntnisse der dynamischen Interaktion zwischen C. cinerea Hyphen und dem Gram-positiven Bakterium Bacillus subtilis gewonnen werden. Diese Bakterien hafteten polar an bestimmten C. cinerea Hyphen und zeigten eine antifungale Wirkung auf einzelne Hyphen. Das dritte Kapitel beschreibt die Identifikation und die biochemische Charakterisierung von zwei paralogen intrazellulären Pilzproteinen. Diese Proteine konnten N-acyl-Homoserin Laktone, Quorum Sensing Moleküle Gram-negativer Bakterien, hydrolysieren. Wenn C. cinerea Hyphen zusammen mit den Quorum Sensing Molekülen inkubiert wurden, nahm die Konzentration von den Quorum Sensing Molekülen über Zeit im Überstand ab. Die zwei pilzlichen Proteine waren homolog zu bekannten bakteriellen Laktonasen. Die Verteilung von Laktonase Genen in den Genomen von Ständerpilzen wurde mit dem Lebensstil dieser Pilze korreliert. Das vierte Kapitel beschreibt die vergleichende Transkriptom-Studie des vegetativen Myzels von C. cinerea, das entweder in Gegenwart des Gram-positiven Bakteriums B. subtilis oder des Gram-negativen Bakteriums Escherichia coli gezüchtet wurde. C. cinerea zeigte auf beide bakteriellen Spezies eine überlappende Antwort wobei Gene, die für sekretierte Proteine kodieren, vermehrt induziert waren. Einige dieser Proteine konnten im Bakterien-induzierten Sekretom mit Hilfe von Shotgun Proteomics nachgewiesen werden. Eine Familie von Lysozymen und Defensin ähnlichen Proteinen und deren antibakterielle Wirkung gegen Gram-positive Bakterien wurde näher untersucht. Das fünfte Kapitel charakterisiert eines der Bakterien-induzierten Gene, das in Kapitel vier identifiziert wurde. Es konnte bestätigt werden, dass dessen Genprodukt in der Biosynthese des antibakteriellen Sekundärmetaboliten Lagopodin B involviert ist. Lagopodin B wurde hergestellt, wenn C. cinerea zusammen mit Bakterien oder deren zellfreien Überstand kultiviert wurde. C. cinerea exprimierte dieses Gen in der Gegenwart von Gram-positiven und Gramnegativen Bakterien, obwohl der Sekundärmetabolit nur gegen Gram-positive Bakterien wachstumsinhibierende Aktivität zeigte. Mit Hilfe der entwickelten Methode, die im Kapitel ii
5 zwei beschrieben wurde, und der Anwendung eines Reporterstammes wurde die Lokalisation der Expression dieses Genes auf zellulärer Ebene untersucht. Das sechste Kapitel enthält eine zusammenfassende Schlussfolgerung und einen Ausblick für zukünftige Forschung im Bereich der pilzlichen Abwehr gegen bakterielle Antagonisten. iii
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