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Vibrio Parahaemolyticus Transcriptional regulation by sigma factor phosphorylation controls polymyxin resistance and swarming behavior in Vibrio parahaemolyticus DISSERTATION zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) dem Fachbereich Biologie der Philipps-Universität Marburg vorgelegt von SHANKAR CHANDRASHEKAR IYER aus Chennai, India Marburg/Lahn im Juni 2019 Originaldokument gespeichert auf dem Publikationsserver der Philipps-Universität Marburg http://archiv.ub.uni-marburg.de Dieses Werk bzw. Inhalt steht unter einer Creative Commons Namensnennung Keine kommerzielle Nutzung Weitergabe unter gleichen Bedingungen 3.0 Deutschland Lizenz. Die vollständige Lizenz finden Sie unter: http://creativecommons.org/licenses/by-nc-sa/3.0/de/ Die Untersuchungen zur vorliegenden Arbeit wurden von Oktober 2015 bis Juli 2019 am Max-Planck-Institut für Terrestrische Mikrobiologie unter der Leitung von Dr. Simon Ringgaard durchgeführ. Vom Fachbereich Biologie der Philipps-Universität Marburg als Dissertation angenommen am: Erstgutachter: Dr. Simon Ringgaard Zweitgutachter: Prof. Dr. Anke Becker Weitere Mitglieder der Prüfungskommission: Prof. Dr. Gert Bange Prof. Dr. Hans-Ulrich Mösch Tag der mündlichen Prüfung am: 06.09.2019 Die während der Promotien erzielten Erbebnisse wurden zum Teil in folgenden Originalpublikationen veröffentlicht: Shankar Chandrashekar Iyer, Delia Casas-Pastor, David Kraus, Petra Mann, Kathrin Schirner, Timo Glatter, Georg Fritz, and Simon Ringgaard Transcriptional regulation by σ factor phosphorylation in bacteria. Nature Microbiology. In revision. To Amma, Appa and my dear Kat Table of Contents _______________________________________________________________ Table of Contents ABBREVIATIONS ........................................................................................................... 11 ABSTRACT ..................................................................................................................... 13 ZUSAMMENFASSUNG .................................................................................................. 14 1. CHAPTER 1: INTRODUCTION .............................................................................. 15 1.1. Post-translational modifications ...................................................................... 16 1.1.1. Phosphorylation as a post-translational modification ............................... 17 1.2. Protein kinases................................................................................................ 18 1.2.1. Discovery of protein kinases in eukaryotes ................................................ 18 1.2.2. Discovery of protein kinases in bacteria ................................................... 19 1.2.3. Classification of kinases: Chemical nature of the side chains ................. 19 1.2.4. The high energy phosphate donor............................................................ 20 1.2.5. Protein kinases as drug targets ................................................................ 20 1.2.6. Structure of eukaryotic protein kinases .................................................... 20 1.2.6.1. cAPK has a bi-lobed structure ........................................................... 21 1.2.6.2. Distinct features of cAPK that are required for its activity................. 22 1.2.6.2.1. The catalytic domain .................................................................... 22 1.2.6.2.2. The activation loop ....................................................................... 22 1.2.7. Kinases in bacteria.................................................................................... 24 1.2.7.1. Two component systems (TCS) ........................................................ 24 1.2.7.2. Phosphotransferases......................................................................... 24 1.2.7.3. Serine/threonine kinases (STKs) ...................................................... 25 1.2.7.3.1. Comparison of STKs to TCS........................................................ 25 1.2.7.3.2. Structure of bacterial STKs .......................................................... 25 1.2.7.3.3. A model for allosteric activation within STKs in bacteria ............. 26 1.2.7.3.3.1. Ligand-based dimerization .................................................... 26 1.2.7.3.3.2. Activation through transphosphorylation .............................. 27 1.2.7.3.4. C-terminal domains of STKs ........................................................ 27 1.2.7.3.5. Evolution of STKs......................................................................... 28 1.2.7.3.6. Biological roles for Ser/Thr kinases ............................................. 28 1.2.7.3.6.1. Interaction with two component systems .............................. 29 1.2.7.3.6.2. Regulation of transcriptional factors ..................................... 30 1.2.7.3.6.3. Regulation of protein synthesis............................................. 31 1.2.7.3.6.4. Roles in cell wall synthesis ................................................... 31 1.2.7.3.6.5. Roles in cell morphology, division and development ........... 32 1.2.7.3.6.6. Roles in central metabolism .................................................. 34 1.2.7.3.6.7. Roles in virulence and pathogenicity .................................... 35 1.2.7.4. Dual specificity protein kinases ......................................................... 36 Table of Contents _______________________________________________________________ 1.3. Transcription in bacteria .................................................................................. 38 1.3.1. Components of the RNA polymerase ....................................................... 38 1.3.2. Structural studies on the RNA polymerase ............................................... 39 1.4. Sigma factors................................................................................................... 40 1.4.1. Discovery and key features of σ factors ................................................... 40 1.4.2. Sigma factors are important for promoter recognition .............................. 41 1.4.3. σ54 family of σ factors................................................................................. 41 1.4.4. σ70 family of σ factors ................................................................................ 42 1.4.4.1. Classification of the σ70 family ............................................................ 42 1.4.5. The different regions of σ factors .............................................................. 43 1.4.6. Interaction of the σ factor with the RNA polymerase ................................ 44 1.4.7. Molecular dynamics enabling promoter recognition and melting by σ factors 46 1.4.8. ECF sigma factors ..................................................................................... 47 1.4.8.1. Identification of ECF σ factors ........................................................... 47 1.4.8.2. Principle roles of ECF σ factors ......................................................... 48 1.4.8.3. Interactions of the ECF σ factor with the promoter DNA and the RNA polymerase .......................................................................................................... 49 1.4.8.4. Regulation of ECF σ factors .............................................................. 49 1.4.8.4.1. Regulated proteolysis ................................................................... 50 1.4.8.4.2. Conformational changes within the anti-σ factor ......................... 52 1.4.8.4.2.1. Mechanism of inhibition of ECF σ factors by anti-σ factors .. 53 1.4.8.4.3. Regulation by interactions with other proteins ............................. 54 1.4.8.4.4. Regulation by partner switching mechanism ............................... 55 1.4.8.4.5. C-terminal extensions within the σ factor ..................................... 57 1.4.8.4.6. Through transcriptional activation ................................................ 57 1.4.8.5. Classification of ECF σ factors .......................................................... 58 1.4.8.6. Functions of ECF σ factors ................................................................ 60 1.4.8.6.1. Pathogenecity ............................................................................... 60 1.4.8.6.2. Developmental processes ............................................................ 60 1.4.8.6.3. Responses to different extracellular stresses .............................. 61 1.4.8.6.3.1. Heat shock ............................................................................. 61 1.4.8.6.3.2. Iron starvation ........................................................................ 61 1.4.8.6.3.3. Antibiotic stress...................................................................... 61 1.4.8.6.3.4. ECF σ factors often sense multiple external stresses .......... 62 1.5. Vibrio parahaemolyticus as a model organism ............................................... 63 2. Chapter 2: Aim and Scope ...................................................................................... 65 3. Chapter 3: Regulation of ECF σ factor through phosphorylation in bacteria ......... 71 3.1. Introduction ...................................................................................................... 73 3.2. Results ............................................................................................................. 75 3.2.1. ECF σ factor phosphorylation in bacteria ................................................
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