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Investigations on Halobacterial Transducers with Respect to Membrane Potential Sensing and Adaptive Methylation

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Investigations on Halobacterial Transducers with Respect to Membrane Potential Sensing and Adaptive Methylation Investigations on halobacterial transducers with respect to membrane potential sensing and adaptive methylation Dissertation zur Erlangung des Doktorgrades der Fakultät für Chemie und Pharmazie der Ludwig-Maximilians-Universität München Matthias Koch aus Eschwege 2005 Erklärung: Diese Dissertation wurde im Sinne von § 13 Abs. 3 bzw. 4 der Promotionsordnung vom 29. Januar 1998 von Prof. Dr. Dieter Oesterhelt betreut. Ehrenwörtliche Versicherung: Diese Dissertation wurde selbstständig, ohne unerlaubte Hilfe angefertigt. München, 25.08.2005 ....................................... (Matthias Koch) Dissertation eingereicht am 9.9.2005 1. Gutachter: Prof. Dr. Dieter Oesterhelt 2. Gutachter: Prof. Dr. Karl-Peter Hopfner Mündliche Prüfung am 14.12.2005 This dissertation was generated between October 1999 and August 2005 at the Max-Planck Institute of Biochemistry in Martinsried, in the Department of Membrane Biochemistry under the guidance of Prof. Dr. Dieter Oesterhelt. Parts of this work were previously published: Poster presentation at the International Conference on Halophilic Microorganisms, Sevilla, Spain, September 23 - 27, 2001 Poster presentation at the Gordon Research Conference on Sensory Transduction In Microorganisms, Ventura, CA, USA, January 11 - 16, 2004 Koch, M.K., and Oesterhelt, D. (2005) MpcT is the transducer for membrane potential changes in Halobacterium salinarum. Molecular Microbiology 55: 1681-1694. Sprüche des Konfuzius Dreifach ist des Raumes Maß: Rastlos fort ohn Unterlaß Strebt die Länge; fort ins Weite Endlos gießet sich die Breite; Grundlos senkt die Tiefe sich. Dir ein Bild sind sie gegeben: Rastlos vorwärts mußt du streben, Nie ermüdet stillestehn, Willst du die Vollendung sehn; Mußt ins Breite dich entfalten, Soll sich dir die Welt gestalten; In die Tiefe mußt du steigen, Soll sich dir das Wesen zeigen. Nur Beharrung führt zum Ziel, Nur die Fülle führt zur Klarheit, Und im Abgrund wohnt die Wahrheit. Friedrich Schiller (1759-1805) TABLE OF CONTENTS Table of Contents 1 SUMMARY...............................................................................................................................1 2 INTRODUCTION....................................................................................................................5 2.1 The halophilic archaeon Halobacterium salinarum............................................................5 2.1.1 Taxonomy, ecology and metabolic properties..................................................................5 2.1.2 Morphology and swimming behavior...............................................................................7 2.2 Signal transduction and taxis in bacteria and archaea......................................................8 2.2.1 Histidine-aspartate phosphorelay (HAP) systems are an integral part of most common prokaryotic sensory pathways......................................................................................9 2.2.2 The molecular machinery mediating enterobacterial signal transduction as a paradigm of prokaryotic signaling systems...............................................................................10 2.2.3 Transducers relay external stimuli to the cell interior, and changes in their methylation status are involved in adaptation to a given stimulus intensity.............................14 2.3 Halobacterial signal transduction at a molecular level....................................................18 2.3.1 The halobacterial Che protein machinery displays similarities to that of B. subtilis......18 2.3.2 Halobacterial transducers are class III transducers involved in sensing a variety of stimuli....................................................................................................................20 2.3.3 Methylation of Htrs.........................................................................................................21 2.4 Bacteriorhodopsin-dependent phototaxis in H. salinarum..............................................22 2.4.1 The proton motive force (pmf)........................................................................................23 2.4.2 Hints towards an involvement of the signaling chain.....................................................23 2.5 Objectives of the thesis........................................................................................................25 3 RESULTS AND DISCUSSION.............................................................................................26 3.1 Identification of MpcT (Htr14) as the transducer for ∆Ψ changes in H. salinarum.....26 3.1.1 Construction of retinal-protein knockout strains ............................................................26 3.1.2 Transducer inventory of H. salinarum............................................................................29 3.1.3 Generation of htr-deletions in strains MKK101 and MKK102......................................31 3.1.4 Red-blue colony selection as a new method facilitating the screening of halobacterial transformants.......................................................................................................32 3.1.5 BR-dependent phototaxis is mediated by Htr14 and involves stimulus-induced methanol release........................................................................................................................34 3.1.6 Htr14 is also responsible for HR-dependent photoresponses.........................................36 3.1.7 Htr14 is bound to the plasma membrane and can exist in differently methylated forms.......................................................................................................................37 3.1.8 Mass spectrometrical analysis identified four methylatable residues in Htr14 and suggests a set of Htr14 species consistent with that seen on immunoblots........................39 i TABLE OF CONTENTS 3.1.9 The buffering capacity of the H. salinarum cytoplasm argues for a change in ∆Ψ as the stimulus that is sensed via Htr14....................................................................................42 3.1.10 MpcT (Htr14) by itself probably serves as the ∆Ψ sensor............................................46 3.1.11 Structural and clustering model for E. coli Tsr and MpcT............................................50 3.1.12 Summary of MpcT (Htr14) action and outlook............................................................59 3.2 Mass spectrometrical identification of methylation sites in Htrs....................................62 3.2.1 Starting point and strategy for the investigation of Htr methylation...............................62 3.2.2 An evaluation of MALDI-TOF MS experiments provided first hints towards the detectability of methylated peptides via MS.............................................................................65 3.2.3 LC ESI Q-TOF MS(/MS) after in-gel Asp-N digestion of the respective Htrs is the method of choice to investigate Htr-methylation............................................................67 3.2.4 Mascot MS/MS ions searches with the detected peptide fragment masses identified differently methylated forms of certain Htr peptides................................................70 3.2.5 For a number of Htrs either the methylation sites or the individual methylated residues could be identified via tandem MS (MS/MS).............................................................74 3.2.6 MS/MS spectra can provide different levels of information concerning the methylation of transducer peptides...........................................................................................77 3.2.7 Deamidations at position 2 of heptad -11 of Htr4 and Htr15 only in wild-type but not in the ∆cheB strain identify CheB as the deamidase of H. salinarum..........................82 3.2.8 Methylation sites within the methylatable regions of membrane-bound Htrs were identified in heptads -13, -12, +13, +15 and +17......................................................................83 3.2.9 Transducer evolution could be explained by a scenario different from the insertion/deletion (indel)-hypothesis.........................................................................................86 3.2.10 An additional methylatable site was identified in the signaling region of Htr14 (MpcT) in heptad +2.................................................................................................................89 3.2.11 Summary of Htr methylation and outlook.....................................................................90 4 MATERIALS AND METHODS...........................................................................................94 4.1 Chemicals and enzymes.......................................................................................................94 4.1.1 Chemicals........................................................................................................................94 4.1.2 Kits and Enzymes............................................................................................................95 4.2 Microbiological materials and methods.............................................................................96 4.2.1 Strains and culture conditions.........................................................................................96 4.2.2 Plasmids..........................................................................................................................99 4.2.3 Media and antibiotics....................................................................................................101
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