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Regulation of the General Stress Response of Bacillus Subtilis Regulation of the General Stress Response of Bacillus subtilis Dissertation zur Erlangung des akademischen Grades Doktor-Ingenieur (Dr.-Ing.) Promotionsgebiet Systembiologie Fakult¨at fur¨ Informatik und Elektrotechnik Universit¨at Rostock vorgelegt von Ulf W. Liebal, geboren am 15. September 1981 in Magdeburg/Elbe Rostock/Warnow, 25. September 2012 F¨ur Uta Nast The cover picture is the truncated icosahedron by Luca Pacioli, De divina proportione, 1509, on page XXIIII. The truncated icosahedron is the geometric structure underlying the stressosome protein complex, and which provides the basis of the cellular automata developed in Chapter 3 and Chapter 4. Ich wollte ihn auf die Probe stellen: “und was ist Zwei mal Zwei?” Er: “Der L¨ugner w¨urde behaupten f¨unf - der Neutrale weder zwei noch sechs - der vorsichtige Esoteriker w¨urde sich ¨außern: Logarithmus 10 000 oder so.” “Wie w¨are es mit 4”, schlug ich ver¨achtlich vor. “Das sind die ausgesprochenen Fanatiker. Klavki! Rationalismus ist: Wahrheitskonsum.” Der Wolkenh¨andler, Klavki Danksagung Es war eine erf¨ullende Zeit in Rostock und am Lehrstuhl Systembiologie und Bioinfor- matik. Diese M¨oglichkeit verdanke ich Olaf Wolkenhauer, der mir die Gelegenheit und das Vertrauen gegeben hat in seiner Gruppe zu forschen. Ich danke dir f¨ur die Freiheit, mit der ich meine, nicht immer zielgerichteten, Ideen verfolgen konnte. Deine Geduld und dein Vertrauen mit meinem ‘Verfolgen’ waren formend f¨ur meine Entwicklung. Thomas Millat hat die wichtige t¨agliche Arbeit verrichtet, mich mit der Realit¨atzu verbinden. Deine strengen Anforderungen an eine wissenschaftliche Arbeitsweise waren eine Herausforderung f¨ur mich, aber sie haben meine Aufmerksamkeit f¨urdas Detail gesch¨arft. Du warst immer erreichbar, und wir konnten ¨uber viele Themen diskutieren. Die Zeit mit Peter Raasch war zu kurz. So viele Themen schwebten zwischen unseren Tischen ... Deine Partikel Simulation ist bisher unerreicht und ein wichtiger Bestandteil meiner Arbeit. Das Orpheusprojekt war leider erfolglos und ich hoffe, dass du ein anderes Rad zur Schwingung findest. Ich hoffe auch wieder einen Tango mit Yvonne Schmitz zu tanzen, doch f¨urchte ich, dass du nur einfach wieder deinen Kopf wegdrehst, gerade wenn ich dich anspreche. Viele Ulfs gibt es nicht, und dann gleich zwei in einer Gruppe ... ohne unsere Wettstreits w¨aren es einige Schmunzler weniger gewesen. Felix Winter stimulierte die Entwicklung der Zellul¨arenAutomaten und ich danke Stefan Pauleweit f¨ur die gelungenen Photos der Papierstressosoms. Herr Uwe V¨olker hat das Gesamtprojekt aus Greifswald koordiniert. Seine Objektivit¨at, und Geradlinigkeit sind bewundernswert. Die von ihm geleiteten Diskusionen endeten immer in einem konkreten Ergebnis. Die verst¨andnisvolle Art und ruhige Aura von Leif Steil hat die Zusammenarbeit mit ihm besonders angenehm gestaltet. For a while, I was sitting two armlengths apart from Julio Vera Gonz´alez. It was wonderful to listen to your stories, the revolutions, and conspiracies all around. With Anuradha Chauhan I had the most challenging discussions, but it was good to relax during your group-Yoga initiative. It was very stimulating that each of us, Angie Lao, Xin Lai, and me prepared our theses simultaneously, but more will I remember our tranquil gatherings in the kitchen when time seemed to stop. Praveen K. Sappa and in the beginning Hendrikje Hildisch provided the experiments for my models, resulting in the Chapter 5. Praveen, we had good times on the conferences, I hope we don’t get too old for Amsterdam. Newcastle is among the best cities I have seen, but that is for a big part because of Rick Lewis and Jon-Marles Wright. I enjoyed the time there so much, you gave me such a great hospitality! But also in distance, working with you was fabulous, your comments on the manuscripts were staggeringly precise and your responses rapid. Oscar Kuipers, Imke van Baarle, and Georg Homuth, as well as Anja M¨oller and Dinto Jos´ehelped me to improve my manuscripts. I am indebted to helpful corrections on the thesis to Anuradha Chauhan, Wiebke Chemnitz, Sherry Freiesleben, Jiri Jablonski, Thomas Millat, Julio Vera, and Florian Wendland. Wissenschaft darf nicht im Elfenbeinturm bleiben, und ich bin Wolfang Thiel dankbar, dass wir zusammen einen allgemeinen Artikel an die Zeitungen brachten. Die Bastelkunst der Geigenbauerin Theresa L¨ucking hat mich auf die Origammitechnik f¨urIkosaheder aufmerksam gemacht. Das war eine wichtige Ambition f¨urdie Entwicklung der Stressosom- Modelle. Die Zeit in Rostock war vorallem auch so sch¨ondurch das Musizieren im FSOR. Ich danke Ines Steinhagen, Juliane Werlich, Christina Fl¨agel, Martin Wollmann, Konrad Jakobi f¨ur die Vorstandssitzungen und Maria Dreier f¨ur das gemeinsame Musizieren am Fagott. Ich danke meiner Familie f¨urdie Unterst¨utzung. Daf¨ur, dass ich bei Familie Sch¨oning entspannen kann, und die Hausmusiken bei Winfried Liebal. Der tiefste Dank geht an Uta Nast-Schneider. Es hat gedauert, bis ich begriff, dass man kann kein Lieblingstier haben kann, da alles ineinandergreift. Die erstrebenswerte Aufopferung im Professionellen wie im Privaten von Ludwig Nast sind verbunden mit einer sympatischen Ausgeglichenheit, Gutm¨utigkeit und geistigen St¨arke. Es war eines seiner Herzensw¨unsche die Fertigstellung dieser Arbeit mitzuerleben. Leider blieb Ludwig Nast dazu nicht die Zeit. Ich danke dem BMBF f¨urdie Finanzierung durch die BaCell und BaCell2 SysMO Pro- jekte (FKZ: 0313978 and 0315784). Abstract The bacterium Bacillus subtilis lives in the environmentally diverse soil habitat. Various stresses challenge B. subtilis, and its stressosome is one of the sensors for physical and chemical insults. This pseudo-icosahedral complex is composed of three protein classes: 1) the sensor RsbR, 2) the scaffold RsbS, and 3) the kinase RsbT. Stimulation of the stressosome modifies its phosphorylation patterns and protein interactions, and results in the dissociation of RsbT. Cytoplasmic RsbT activates an additional cascade, ultimately releasing the general stress response transcription factor σB. Biochemical and molecu- lar biological experiments have identified the reactions and interactions of the proteins, but these techniques are currently unable to identify structure-related functions. By con- trast, computational models can consider the geometry of the stressosome, but despite this advantage, no such model exists for the stressosome. Using cellular automata, I introduce here the first computational models for the stressosome. Futhermore, the icosa- hedral structure enables the construction of a geometric model by modular origami folding that highlights motions within icosahedral structures. The conditions associated with the release of σB are amenable to ordinary differential equation models, which I used to re- produce the dynamics of a reporter protein. My analysis shows that different stimuli are processed identically, suggesting their identical perception. Theoretical reproduction of the dynamics of a reporter protein show that the proteolytic decay of the reporter protein is part of the σB-mediated general stress response, which was confirmed by subsequent experiments. The thesis confirms the activation effect of RsbR-P on the kinase activity of RsbT and the preferential dephosphorylation of RsbS-P over RsbR-P by RsbX. The Collapse Hypothesis suggested in this thesis, concerns information transmission between RsbR and RsbT and suggests a coordinated motion of three dimers. The modelling pro- cess emphasizes an activation loop for RsbT that disconnects the duration of response from that of the stimulus. Overall, the new insights enhance our understanding of the σB- mediated general stress response and raise our awareness of the environmental integration of B. subtilis. Zusammenfassung Das Bakterium Bacillus subtilis lebt im Boden und ist dort verschiedenen Umweltreizen ausgesetzt. Ein Teil dieser Reize wird durch das Stressosom aufgenommen. Diese komplexe Struktur von pseudo-ikosahedraler Geometrie besteht aus drei Proteinklassen: 1) dem Sen- sor RsbR, 2) dem Gerustprotein¨ RsbS und 3) der Kinase RsbT. Durch Stimulation des Stressosoms ver¨andert sich sein Phosphorylierungsmuster, was die Interaktionen der Pro- teine ver¨andert und zur Dissoziation von RsbT fuhrt.¨ Das frei-werdende, cytoplasmatische RsbT aktiviert eine weitere Signalkaskade, die schließlich zur Freisetzung des Transkrip- tionsfaktors σB und zur allgemeinen Stressantwort fuhrt.¨ Durch biochemische und mo- lekularbiologische Ans¨atze konnten die Reaktionen und Interaktionen aufgekl¨art werden, jedoch sind diese Techniken ungeeignet, Informationen zu strukturbezogenen Funktionen zu liefern. Obwohl im Gegensatz mathematische Modelle die Geometrie des Stressosoms berucksichtigen¨ k¨onnen, gab es bisher noch kein Modell zum Stressosom. In dieser Ar- beit stelle ich die ersten rechnerbasierten Modelle zum Stressosom auf Basis zellul¨arer Automaten vor. Zus¨atzlich kann dessen ikosahedrale Struktur durch ein geometrisches Model auf Basis von Origammi-Falttechniken reproduziert werden, was Informationen zu Dom¨anenbewegungen liefert. Die Bedingungen der Freisetzung von σB erlauben die An- wendung von Differentialgleichungen, mit denen ich die Dynamik eines Reporterproteins nachvollziehe. Meine Analysen zeigen, dass unterschiedliche Signale identisch verarbeitet werden, was nahelegt, dass diese Signale auch identisch aufgenommen werden. Die theore- tische Reproduktion einer Reporterproteindynamik zeigt, dass der proteolytische Abbau
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