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The Intracellular Behaviour of Burkholderia Cenocepacia in Murine Macrophages

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The Intracellular Behaviour of Burkholderia Cenocepacia in Murine Macrophages Western University Scholarship@Western Electronic Thesis and Dissertation Repository 11-28-2011 12:00 AM The intracellular behaviour of Burkholderia cenocepacia in murine macrophages Jennifer S. Tolman The University of Western Ontario Supervisor Dr. Miguel A. Valvano The University of Western Ontario Graduate Program in Microbiology and Immunology A thesis submitted in partial fulfillment of the equirr ements for the degree in Doctor of Philosophy © Jennifer S. Tolman 2011 Follow this and additional works at: https://ir.lib.uwo.ca/etd Part of the Cell Biology Commons, Genetics Commons, and the Microbiology Commons Recommended Citation Tolman, Jennifer S., "The intracellular behaviour of Burkholderia cenocepacia in murine macrophages" (2011). Electronic Thesis and Dissertation Repository. 338. https://ir.lib.uwo.ca/etd/338 This Dissertation/Thesis is brought to you for free and open access by Scholarship@Western. It has been accepted for inclusion in Electronic Thesis and Dissertation Repository by an authorized administrator of Scholarship@Western. For more information, please contact [email protected]. THE INTRACELLULAR BEHAVIOUR OF BURKHOLDERIA CENOCEPACIA IN MURINE MACROPHAGES (Spine title: Intramacrophage behaviour of B. cenocepacia) (Thesis format: Monograph) by Jennifer Sarah Tolman Graduate Program in Microbiology and Immunology A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy The School of Graduate and Postdoctoral Studies The University of Western Ontario London, Ontario, Canada © Jennifer S. Tolman 2012 THE UNIVERSITY OF WESTERN ONTARIO School of Graduate and Postdoctoral Studies CERTIFICATE OF EXAMINATION Supervisor Examiners ______________________________ ______________________________ Dr. Miguel Valvano Dr. France Daigle Supervisory Committee ______________________________ Dr. Charles Trick ______________________________ Dr. John McCormick ______________________________ Dr. Susan Koval ______________________________ Dr. Lina Dagnino ______________________________ Dr. Peter Cadieux The thesis by Jennifer Sarah Tolman entitled: The Intracellular Behaviour of Burkholderia cenocepacia in Murine Macrophages is accepted in partial fulfillment of the requirements for the degree of Doctor of Philosophy ______________________ _______________________________ Date Chair of the Thesis Examination Board ii Abstract Burkholderia cenocepacia is an opportunistic pathogen causing life-threatening infections in cystic fibrosis and other immunocompromised patients. The bacterium survives within macrophages by interfering with typical endocytic trafficking, resulting in delayed maturation of a B. cenocepacia-containing phagosome. We hypothesize that B. cenocepacia alters gene expression after internalization by macrophages, inducing genes involved in intracellular survival and host adaptation. Furthermore, we hypothesize that specialized bacterial secretion systems are involved in the interactions between intracellular bacteria and macrophages. In this work, we characterize later-stage infection of macrophages by B. cenocepacia, showing replication within an acidified endosomal compartment suggestive of a phagolysosome. We examine differential gene expression by intracellular B. cenocepacia using selective capture of transcribed sequences (SCOTS) with both competitive enrichment and microarray analysis. We identified 766 genes differentially regulated in intracellular bacteria, of which 329 were induced and 437 repressed. Affected genes are involved in all aspects of cellular life, including information storage and processing, cellular processes and signalling, and metabolism; in general, intracellular gene expression demonstrates a pattern of environmental sensing, bacterial response, and metabolic adaptation to the phagosomal environment. Deletion of various SCOTS-identified genes affects B. cenocepacia entry into macrophages and intracellular replication, as well as host-directed cytotoxicity and spread to neighbouring cells. Expression of secretion system genes is iii differentially-regulated by intracellular B. cenocepacia. Although none of the five major secretion systems are essential for growth in culture, we show that bacterial secretion systems are involved in macrophage entry, intracellular replication, and host-directed cytotoxicity. Type IV secretion systems play a role in early interactions with macrophages, while type II and VI secretion systems contribute to post-internalization intracellular replication and host-directed cytotoxicity. As a whole, secretion systems appear to increase pathogenicity in macrophages while limiting the spread of B. cenocepacia infection. Together, these studies advance our understanding of the intracellular behaviour of B. cenocepacia in macrophages. Further investigation into the remaining SCOTS-identified genes, as well as putative secreted effectors, will provide a better understanding of the adaptive responses of intracellular B. cenocepacia, leading to life in a phagosomal niche and host cell cytotoxicity. Keywords Burkholderia cenocepacia, macrophage, intracellular gene expression, microarray, SCOTS, secretion systems iv Acknowledgments Reaching this final step in the Ph.D. program would not have been possible without the assistance and input of a great many people, to whom I owe a great deal of thanks. First of all, to my supervisor, Dr. Miguel Valvano: Thank you for taking a chance on a last minute e-mail and accepting an NSERC summer student that turned into a five year grad student. It’s been a long road, but I’ve learned a great deal. You’ve created an environment that fosters scientific curiosity, collaboration and creativity, and I’ve enjoyed the past five years. To my advisory committee, Dr. John McCormick and Dr. Lina Dagnino: I really appreciate you taking time out of your busy schedules to offer a fresh perspective and helpful suggestions. Our meetings were of great benefit to my studies. To Dr. Ximena Ortega: You showed me what real microbiology looks like. Thanks for introducing me to the world of Burkholderia, and teaching me how to do a mean chromosome prep and Southern blot along the way. To Dr. Mohamad Hamad: My official plate-taker-outer, and general science cheerleader! Your tips, tricks, and scientific innovations made my life so much easier. Plus, you made it fun to be at the Burkholderia end of the lab! To Dr. Susan Koval: Five years of TA-ing Biology of Prokaryotes! It has been a wonderful experience, and I’ve learned as much as my students! To Judy Sholdice (& Dr. Susan Koval): Thanks for letting me play with the EM! To Dr. Andrea Sass (& Dr. Eshwar Mahenthiralingam): Thank you for figuring out how to apply my SCOTS cDNA to the J2315 arrays. v To Dr. Kristin Chadwick & Dr. Karen Morley: Thanks for teaching me all about flow cytometry, and for running over to SDRI to troubleshoot whenever the need arose. To Jennifer Brace: For dealing with all the bureaucracy and paperwork so that I didn’t have to, I offer my most sincere thanks! To everyone in the lab, especially Ximena, Ron, Sole, Dan, Mo, Slade, Cristina, Julie, Karen, Kendra, Kina, Sarah, Crystal, Roberto, Omar, and Katie: You made it fun to come to work! Thanks for answering questions, celebrating the successes, and figuring out how to fix the failures. In the words of Roberto & Mo, “Teamwork! Sci-ence!” Last, but certainly not least, to my family: I can never say thank you enough for all your love, support, and encouragement, and for putting up with me through the “summer of the thesis”. I couldn’t have done it without you! Lots of love, Jenni. vi Table of Contents CERTIFICATE OF EXAMINATION ...................................................................... ii Abstract ................................................................................................................iii Acknowledgments ................................................................................................ v Table of Contents ................................................................................................vii List of Tables ......................................................................................................xiv List of Abbreviations ...........................................................................................xix Chapter 1 – Introduction ....................................................................................... 1 1.1 Burkholderia cenocepacia and the Burkholderia cepacia complex ............ 1 1.1.1 The Burkholderia cepacia complex ................................................. 1 1.1.2 Burkholderia cenocepacia............................................................... 2 1.1.3 B. cenocepacia in the environment ................................................. 3 1.1.3.1 Phytopathogens ................................................................. 3 1.1.3.2 Beneficial interactions with plants....................................... 4 1.1.3.3 Endosymbiosis with insects................................................ 5 1.1.3.4 Bioremediation ................................................................... 6 1.1.3.5 Commercial potential.......................................................... 6 1.1.4 B. cenocepacia as an industrial contaminant .................................. 7 1.1.5 B. cenocepacia as an opportunistic human pathogen..................... 8 1.1.5.1 Cystic fibrosis ..................................................................... 9 1.1.5.2 Chronic granulomatous disease......................................
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