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Pore-Forming Proteins in the Outer Membrane of Borrelia Burgdorferi

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Pore-Forming Proteins in the Outer Membrane of Borrelia Burgdorferi PORINS OF LYME DISEASE AND RELAPSING FEVER SPIROCHETES Dissertation zur Erlangung des naturwissenschaftlichen Doktorgrades der Fakultät für Biologie an der Bayerischen Julius-Maximilians-Universität Würzburg vorgelegt von Marcus Thein aus Würzburg Würzburg, 2009 Eingereicht am: ………………………………………….. Mitglieder der Promotionskommission: Vorsitzender: Prof. Dr. …………………. 1. Gutachter: Prof. Dr. Dr. h.c. Roland Benz 2. Gutachter: Prof. Dr. Sven Bergström Tag des Promotionskolloquiums: ………………………………………….. Doktorurkunde ausgehändigt am: ………………………………………….. Diese Dissertation wurde von mir selbständig und nur mit den angegebenen Quellen und Hilfsmitteln angefertigt. Die von mir vorgelegte Dissertation hat noch in keinem früheren Prüfungsverfahren in ähnlicher oder gleicher Form vorgelegen. Ich habe zu keinem früheren Zeitpunkt versucht, einen akademischen Grad zu erwerben. Würzburg, ……………. ………………………… "Natürlicher Verstand kann fast jeden Grad von Bildung ersetzen, aber keine Bildung den natürlichen Verstand." Arthur Schopenhauer Publications Pinne M., Thein M., Denker K., Benz R., Coburn J. and Bergström S. (2007). Elimination of channel-forming activity by insertional inactivation of the p66 gene in Borrelia burgdorferi. FEMS Microbiol Lett 266:241-9. Thein M., Bunikis I., Denker K., Larsson C., Cutler S., Drancourt M., Schwan T. G., Mentele R., Lottspeich F., Bergström S. and Benz R. (2008). Oms38 is the first identified pore-forming protein in the outer membrane of relapsing fever spirochetes. J Bacteriol 190(21):7035-42. Thein M., Bonde M., Bunikis I., Denker K., Sickmann A., Bergström S. and Benz, R. (2008). DipA, a pore-forming protein in the outer membrane of Lyme disease Borrelia exhibits specificity for the permeation of dicarboxylates. Manuscript. Thein M., Bárcena-Uribarri I., Sacher A., Bunikis I., Bergström S. and Benz R. (2008). The P66 porin is present in both Lyme disease and relapsing fever species: a comparison of the biophysical properties of six P66 species. Manuscript. Thein M., Bárcena-Uribarri I., Maier E., Bonde M., Bergström S. and Benz R. (2008). The use of nonelectrolytes as molecular tools reveals the channel size and the oligomeric constitution of the Borrelia burgdorferi porin P66. Manuscript. 7 Table of contents Publications ........................................................................................................................................... 7 Table of contents ................................................................................................................................... 9 Summary ............................................................................................................................................... 15 Zusammenfassung ................................................................................................................................ 18 Chapter 1 – Introduction ......................................................................................................... 23 1.1. The bacterial genus Borrelia ...................................................................... 23 1.1.1. Classification ............................................................................................... 23 1.1.2. General characteristics ............................................................................. 24 1.1.3. Vectors, hosts and life cycle .................................................................... 25 1.1.4. Borrelia and pathogenicity ...................................................................... 26 1.1.5. Species included in this work ................................................................. 27 1.2. The Gram-negative cell-envelope ........................................................... 28 1.2.1. General features of pore-forming outer-membrane proteins (Porins) ....................................................................................... 29 1.3. The Borrelia cell-envelope .......................................................................... 30 1.3.1. Biogenesis and structure of spirochetal outer membrane proteins .................................................................................. 31 1.3.2. Outer surface lipoproteins of Borrelia ................................................. 32 1.3.3. Pore-forming proteins in the outer membrane of Borrelia burgdorferi ................................................................................. 33 1.4. Aims of this work .............................................................................................. 35 Chapter 2 – Oms38 is the first identified pore-forming protein in the outer membrane of relapsing fever spirochetes ..................... 37 2.1. Summary ................................................................................................................ 37 2.2. Introduction ........................................................................................................ 38 2.3. Materials and Methods ................................................................................. 40 9 Table of contents 2.3.1. Bacterial strains and growth conditions ............................................. 40 2.3.2. Isolation of outer membrane proteins and purification of the 38 kDa protein ....................................................... 40 2.3.3. Protein electrophoresis ............................................................................ 40 2.3.4. Protein sequencing ................................................................................... 41 2.3.5. Planar lipid bilayer assays ....................................................................... 41 2.4. Results .................................................................................................................... 42 2.4.1. Pore-forming activities in the outer membrane fractions of B. duttonii, B. hermsii and B. recurrentis .................. 42 2.4.2. Purification and identification of a 38 kDa, pore-forming protein in the outer membranes of B. duttonii, B. hermsii and B. recurrentis ..................................................................................... 43 2.4.3. Analysis of the amino acid sequences of Oms38 of B. duttonii, B. hermsii, B. recurrentis and B. turicatae ................ 44 2.4.4. Single-channel measurements of Oms38 ........................................... 46 2.4.5. Voltage dependence ................................................................................. 48 2.4.6. Selectivity measurements ........................................................................ 48 2.5. Discussion ............................................................................................................ 50 2.5.1. Lipid bilayer experiments with outer membrane fractions (OMFs) of RF species suggest the presence of porins ................. 50 2.5.2. Purification and identification of Oms38 of B. duttonii, B. hermsii and B. recurrentis ................................................................ 50 2.5.3. Deduced amino acid sequences of Oms38 of B. duttonii, B. hermsii, B. recurrentis and B. turicatae ....................................... 51 2.5.4. Biophysical properties of Oms38 .......................................................... 52 Chapter 3 – DipA, a pore-forming protein in the outer membrane of Lyme disease spirochetes exhibits specificity for the permeation of dicarboxylates .................................................................... 55 3.1. Summary ................................................................................................................ 55 3.2. Introduction ......................................................................................................... 56 3.3. Materials and Methods ................................................................................. 58 3.3.1. Bacterial strains and growth conditions ............................................. 58 3.3.2. Isolation of outer membrane proteins and purification of the 36 kDa protein ....................................................... 58 3.3.3. SDS-PAGE and Immunoblotting ......................................................... 58 3.3.4. Overexpression of a recombinant fragment of DipA ...................... 59 3.3.5. Antiserum .................................................................................................... 59 10 Table of contents 3.3.6. Mass spectrometry .................................................................................... 60 3.3.7. Planar lipid bilayer assays ...................................................................... 60 3.4. Results .................................................................................................................... 62 3.4.1. Purification and identification of a new pore-forming protein in the outer membrane of B. burgdorferi ∆p66 ................ 62 3.4.2. Analysis of the DipA amino acid sequences of B. burgdorferi, B. garinii and B. afzelii DipA .................................. 63 3.4.3. Immunoblot analysis of outer membranes and purified B. burgdorferi DipA ................................................................ 64 3.4.4. Single-channel experiments ................................................................... 65 3.4.5. Voltage dependence ................................................................................. 66 3.4.6. Selectivity measurements........................................................................ 67 3.4.7. Inhibition of ion permeation through DipA by addition
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