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Solid Substrate Motility and Phototaxis of the Alpha-Proteobacterium

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Solid Substrate Motility and Phototaxis of the Alpha-Proteobacterium Solid Substrate Motility And Phototaxis Of The Alpha-Proteobacterium, Rhodobacter capsulatus by KRISTOPHER JOHN SHELSWELL Honours B.Sc., University of Waterloo, 2002 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES (Microbiology and Immunology) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) February 2011 © Kristopher John Shelswell, 2011 ABSTRACT The work in this thesis reports the first discovery of flagellum-independent motility in Rhodobacter capsulatus, a purple photosynthetic bacterium. Furthermore, while aqueous swimming motility using a flagellum had been documented, the occurrence of movement over solid and semi-solid substrates had not been reported in R. capsulatus. This motility was found to be affected by the physical and chemical composition of the translocation surface. While motility was reduced under anaerobic (dark) conditions, it did not require oxygen. Cells appeared to respond to multiple stimuli, and were able to move both as coordinated masses and individual cells. Coordinated movements did not require any of the known cell-to-cell communication mechanisms. Movements were influenced by light such that cells usually moved toward a light source over a broad region of the visible spectrum, and this movement appeared to be a genuine phototaxis. A direct linkage between photoresponsive movement and photosynthesis was ruled out, because the photosynthetic reaction center was not required for movement toward white light. Photoresponsive movement occurred independently of the photoactive yellow protein, but appeared to require the bacteriochlorophyll and/or carotenoid pigments. Motility was mediated by flagellum-dependent and flagellum-independent contributions. Flagellum-dependent contributions were responsible for dispersive semi-random movements while flagellum-independent contributions resulted in linear, directed movements. Analysis of several strains indicated that flagellum-independent motility is widespread throughout R. capsulatus. This motility appears to be mediated by a gliding mechanism, perhaps involving the deposition of exopolysaccharide to achieve coordinated cell taxis. ii TABLE OF CONTENTS ABSTRACT ...................................................................................................................................................... ii TABLE OF CONTENTS .................................................................................................................................... iii LIST OF TABLES .............................................................................................................................................. x LIST OF FIGURES .......................................................................................................................................... xii LIST OF ABBREVIATIONS ............................................................................................................................xviii ACKNOWLEDGEMENTS .............................................................................................................................. xix 1. INTRODUCTION ..................................................................................................................... 1 1.1. Rhodobacter capsulatus ................................................................................................................ 1 1.1.1. R. capsulatus taxonomy and characteristics ......................................................................... 1 1.1.2. R. capsulatus genomic characteristics .................................................................................. 1 1.2. Bacterial motility ............................................................................................................................ 2 1.2.1. Adaptive responses ............................................................................................................... 2 1.2.2. Distribution, regulation, and types of bacterial motility ....................................................... 2 1.3. Bacterial flagellum-mediated motility ........................................................................................... 4 1.3.1. Flagellum structure and function .......................................................................................... 4 1.3.2. Aqueous substrate flagellar swimming ................................................................................. 6 1.3.3. Solid substrate flagellar swarming ........................................................................................ 6 1.4. Bacterial pilus-mediated motility .................................................................................................. 7 1.4.1. Pilus structure and function .................................................................................................. 7 1.4.2. Solid substrate pilus twitching ............................................................................................ 10 iii 1.5. Bacterial gliding motility .............................................................................................................. 11 1.5.1. Gliding mechanisms and function ....................................................................................... 11 1.5.2. Cytoskeletal rearrangement in gliding ................................................................................ 11 1.5.3. Extrusion in gliding .............................................................................................................. 13 1.5.4. Focal adhesion in solid substrate gliding............................................................................. 14 1.6. Bacterial sliding motility .............................................................................................................. 15 1.7. Bacterial taxis ............................................................................................................................... 16 1.7.1. Light-responsive motility ..................................................................................................... 16 1.7.2. Energy taxis ......................................................................................................................... 17 1.7.3. Phototaxis ............................................................................................................................ 19 1.7.4. Tactic responses .................................................................................................................. 21 1.8. Research approach to study solid substrate motility in R. capsulatus ........................................ 22 2. MATERIALS AND METHODS ................................................................................................ 24 2.1. Bacterial strains, plasmids, growth conditions, and enumeration of cells .................................. 24 2.2. Bacterial motility assays .............................................................................................................. 33 2.2.1. Design of chambers used for motility assays .............................................................................. 35 2.2.2. Treatment of polystyrene plates used for motility assays .......................................................... 37 2.3. 32P-orthophosphate cell labelling ................................................................................................ 37 2.4. Phase contrast negative stain capsule microscopy ..................................................................... 38 2.5. Phase contrast and Nomarski microscopy ................................................................................... 38 iv 2.6. Cy3 fluorescence microscopy ...................................................................................................... 39 2.7. Transmission electron microscopy .............................................................................................. 39 2.8. SDS-polyacrylamide gel electrophoresis (SDS-PAGE) .................................................................. 40 2.9. Cell surface protein enrichment .................................................................................................. 40 2.10. Protein sequencing ...................................................................................................................... 41 2.11. DNA manipulations ...................................................................................................................... 41 2.12. Alignments and database homology searches ............................................................................ 41 2.13. Construction of mutants .............................................................................................................. 42 2.14. Creation and screening of Tn5 library for flagellum-independent motility deficient mutants ... 46 2.15. Whole cell absorption spectrum ................................................................................................. 46 2.16. RNA isolation and microarray analysis ........................................................................................ 47 2.17. Statistical analysis of cell movement ........................................................................................... 47 3. RESULTS ............................................................................................................................... 49 3.1. Solid substrate motility ...............................................................................................................
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