Fungal lifestyle: analysis of the cell wall and secreted antibacterial proteins
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- Oswalda Busch
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1 DISS. ETH NO Fungal lifestyle: analysis of the cell wall and secreted antibacterial proteins A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) presented by ANDREAS ESSIG MSc ETH Biology born on June 10, 1982 citizen of Mettauertal, Aargau accepted on the recommendation of Prof. Dr. Markus Aebi Dr. Markus Künzler Prof. Dr. Ruedi Aebersold Prof. Dr. Gerald Hart Prof. Dr. Hans-Georg Sahl 2014
2 Summary Fungi and bacteria coexist in a variety of biological niches, including soil, plants, and animals. In these environments, the cell wall and secreted substances provide fungi with an effective machinery to interact and to compete with bacteria. The discovery of penicillin by Alexander Fleming, a fungal antibacterial metabolite, demonstrated the importance of understanding such defense mechanisms. Antimicrobial peptides (AMPs) are a highly diverse group of defense molecules identified in prokaryotes and eukaryotes. As a part of the innate immune system, AMPs act microbicidal and possess immunomodulatory properties. The first chapter provides an overview of the structure and activity of AMPs including pharmaceutical applications. The identification and characterization of a novel fungal AMP is described in chapter 2. Coprinopsis cinerea is a basidiomycete that naturally occurs in herbivorous dung. Based on a defined analytical setup, we studied the interactions of C. cinerea with different bacterial species and analyzed secreted fungal proteins. A novel fungal defensin, copsin, was identified by quantitative mass spectrometry (MS) and recombinantly produced in Pichia pastoris. The structure of copsin was solved by NMR, which revealed an α/β-fold stabilized by six disulfide bonds. Both the structural compactness and its terminal modifications render copsin extremely heat stable and insensitive towards proteases. Characterization of the antibacterial activity showed that copsin acts bactericidal by binding to the cell wall precursor lipid II predominately in Gram positive species. Its high stability and potent activity against bacteria resistant to conventional antibiotics make copsin to a valuable candidate for a novel antibacterial drug. Further characterization of copsin and its homologs is reported in chapter 3. A sequence comparison of copsin exhibited several homologous AMPs encoded in the C. cinerea genome. Copsin and the homologous defensin CC82 were successfully produced in a bioreactor using P. pastoris as the heterologous host. The distinct antibacterial profiles determined for both polypeptides indicate that C. cinerea expresses a diversified group of AMPs against a multitude of microbial competitors found in herbivorous dung. Saprophytic fungi such as C. cinerea secrete an arsenal of enzymes to digest dead organic matter. The secretome of C. cinerea was analyzed by MS, as described in chapter 4. Besides numerous proteases and glycosidases, we discovered a novel lysozyme, for which we optimized the heterologous expression in P. pastoris. This fungal lysozyme has a low sequence identity to known peptidoglycan cleaving enzymes and possesses a very specific antibacterial profile. i
3 The cell wall of fungi is a unique and complex network of polysaccharides and glycoproteins. Besides the function as a determinant of the cell shape, it acts as a protective line for invading and competing microbes. In order to gain more insights in the cell wall structure, we developed a MS based workflow for the analysis of O-mannose (O-Man) glycans, a structurally and functionally important modification of cell wall proteins. In chapter 5, a comprehensive yeast cell wall O-Man glycoproteome is described with an in-depth analysis of the enormous heterogeneity of this type of O-glycosylation. Furthermore, we implemented SILAC (stable isotope labeling by amino acids in cell culture), which is a valuable tool for quantitative MS measurements of O-Man glycans in yeast and other organisms. ii
4 Zusammenfassung Pilze und Bakterien interagieren in einer Vielzahl von biologischen Nischen; einschliesslich dem Erdreich, Pflanzen und Tieren. Dabei dienen die Zellwand und sekretierte Substanzen den Pilzen unter anderem zur Abwehr von Bakterien. Die Entdeckung des pilzlichen Metaboliten Penicillin durch Alexander Fleming und dessen medizinische Anwendung hat gezeigt, wie wichtig das Verständnis solcher Abwehrmechanismen ist. Antimikrobielle Peptide (AMPs) sind eine vielfältige Gruppe von Molekülen, die von Prokaryoten und Eukaryoten exprimiert werden. Als Teil der angeborenen Immunabwehr besitzen AMPs antimikrobielle und immunomodulatorische Eigenschaften. Das erste Kapitel gibt einen Überblick über die Struktur und Aktivität von bekannten AMPs und deren pharmazeutische Anwendungen. Die Identifizierung und Charakterisierung eines neuen pilzlichen AMP wird in Kapitel 2 beschrieben. Coprinopsis cinerea ist ein Ständerpilz, der natürlicherweise auf Dung von pflanzenfressenden Tieren vorkommt. Die Interaktion von C. cinerea mit verschiedenen Bakterienarten wurde in einem Modellsystem studiert, welches es ermöglichte sekretierte Pilzproteine zu analysieren. Dabei wurde das Defensin Copsin mittels quantitativer Massenspektrometrie identifiziert und in Pichia pastoris rekombinant produziert. Die durch NMR gelöste 3D Struktur ergab eine α/β-faltung, die durch sechs Disulfidbrücken stabilisiert ist. Die strukturelle Kompaktheit und die terminalen Modifikationen machen Copsin extrem hitzebeständig und unempfindlich gegenüber Proteasen. Die Charakterisierung der antibakteriellen Aktivität zeigte, dass Copsin an den Peptidoglykan-Vorläufer Lipid II bindet und dabei die Zellwandsynthese von vorwiegend Gram positiven Bakterien hemmt. Die enorme Stabilität und eine starke Aktivität gegen Bakterien, die gegenüber herkömmlichen Antibiotika resistent geworden sind, machen Copsin zu einem vielversprechenden Kandidaten für ein neues Antibiotikum. Die weitere Charakterisierung von Copsin und dessen homologen AMPs wird in Kapitel 3 diskutiert. Ein Sequenzvergleich von Copsin zeigte, dass im Genom von C. cinerea mehrere homologe AMPs kodiert sind. Copsin und das homologe Defensin CC82 wurden erfolgreich in einem Bioreaktor in P. pastoris produziert. Die unterschiedlichen antibakteriellen Profile von Copsin und CC82 deuten darauf hin, dass C. cinerea eine diversifizierte Gruppe von AMPs exprimiert, die gegen spezifische Mikroorganismen aktiv sind. Saprophytisch lebende Pilze wie C. cinerea sekretieren ein Arsenal von Enzymen die dem Abbau von totem organischem Material dienen. Das Sekretom von C. cinerea wurde mittels iii
5 Massenspektrometrie analysiert und ist in Kapitel 4 beschrieben. Unter zahlreichen Proteasen und Glykosidasen identifizierten wir ein neuartiges Lysozym, das wir in P. pastoris heterolog exprimierten. Dieses pilzliche Lysozym zeigt eine niedrige Sequenzidentität mit bereits bekannten Peptidoglykan-spaltenden Enzymen und besitzt ein sehr spezifisches antibakterielles Profil. Die Zellwand von Pilzen ist ein einzigartiges und komplexes Netzwerk von Polysacchariden und Glykoproteinen. Sie dient nicht nur zur Stabilisierung der Zelle, sondern auch zum Schutz vor invasiven und konkurrierenden Mikroben. Basierend auf einem massenspektrometrischen Ansatz haben wir eine Methode zur Analyse von O-Mannose (O-Man) Glykanen entwickelt. Diese O-Glykane stellen eine strukturell und funktionell wichtige Modifikation von Zellwandproteinen dar und ermöglichten uns weitere Einblicke in die Zellwandstruktur. In Kapitel 5 beschreiben wir ein umfassendes Hefe-Zellwand O-Man Glykoproteom und analysieren eingehend die enorme Heterogenität dieser Art von O-Glykosylierung. Zur quantitativen Messung von O-Man Glykanen in Hefe integrierten wir SILAC (stable isotope labeling by amino acids in cell culture) in die Analyse. iv
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