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MOTILITY and CHEMOTAXIS in the LYME DISEASE SPIROCHETE BORRELIA BURGDORFERI: ROLE in PATHOGENESIS by Ki Hwan Moon July, 2016

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MOTILITY and CHEMOTAXIS in the LYME DISEASE SPIROCHETE BORRELIA BURGDORFERI: ROLE in PATHOGENESIS by Ki Hwan Moon July, 2016 MOTILITY AND CHEMOTAXIS IN THE LYME DISEASE SPIROCHETE BORRELIA BURGDORFERI: ROLE IN PATHOGENESIS By Ki Hwan Moon July, 2016 Director of Dissertation: MD A. MOTALEB, Ph.D. Major Department: Department of Microbiology and Immunology Abstract Lyme disease is the most prevalent vector-borne disease in United States and is caused by the spirochete Borrelia burgdorferi. The disease is transmitted from an infected Ixodes scapularis tick to a mammalian host. B. burgdorferi is a highly motile organism and motility is provided by flagella that are enclosed by the outer membrane and thus are called periplasmic flagella. Chemotaxis, the cellular movement in response to a chemical gradient in external environments, empowers bacteria to approach and remain in beneficial environments or escape from noxious ones by modulating their swimming behaviors. Both motility and chemotaxis are reported to be crucial for migration of B. burgdorferi from the tick to the mammalian host, and persistent infection of mice. However, the knowledge of how the spirochete achieves complex swimming is limited. Moreover, the roles of most of the B. burgdorferi putative chemotaxis proteins are still elusive. B. burgdorferi contains multiple copies of chemotaxis genes (two cheA, three cheW, three cheY, two cheB, two cheR, cheX, and cheD), which make its chemotaxis system more complex than other chemotactic bacteria. In the first project of this dissertation, we determined the role of a putative chemotaxis gene cheD. Our experimental evidence indicates that CheD enhances chemotaxis CheX phosphatase activity, and modulated its infectivity in the mammalian hosts. Although CheD is important for infection in mice, it is not required for acquisition or transmission of spirochetes during mouse-tick-mouse infection cycle experiments. However, it has an effect on the survivability of spirochetes in the arthropod vectors. This is the first report of the role of cheD in the host tissue colonization in any pathogenic bacterium. Delineating the role of cheD in B. burgdorferi will provide insights into not only the chemotaxis pathway of this spirochete, but also its asymmetric swimming and infectious life cycle of the spirochete. Chemotaxis signal transduction systems control bacterial motility. Aside from the chemotaxis pathway, the architectural structure of the flagellar apparatus is also intimately intertwined with motility and the morphology of B. burgdorferi. Unlike other externally flagellated bacteria, spirochetes possess periplasmic flagella with a unique structural component called the collar. This unique component is located in the periplasmic space and is linked to the flagellar basal body. However, there are no reports regarding the gene(s) encoding for the collar or its function in any bacterium. In the second project of this dissertation, we have identified for the first time a gene, flbB, in any spirochete, and defined its function in motility, cell morphology, periplasmic flagella orientation, and assembly of other flagellar structures. We also demonstrated the mechanism shown as to how the organism tilts their periplasmic flagella toward the cell pole. MOTILITY AND CHEMOTAXIS IN THE LYME DISEASE SPIROCHETE BORRELIA BURGDORFERI: ROLE IN PATHOGENESIS A Dissertation Presented to The Faculty of the Department of Microbiology and Immunology Brody School of Medicine at East Carolina University In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in Microbiology and Immunology By Ki Hwan Moon July 29, 2016 © Ki Hwan Moon, 2016 Copyright Permission from Individual Journal CHAPTER ONE: Fig. 1.4: Copyright Nature Publishing Group, Nature Reviews Microbiology, 2012 Jan 9; 10(2):87-99. doi: 10.1038/nrmicro2714. Copyright © 2012, Rights Managed by Nature Publishing Group. Fig. 1.5: Copyright Nature Publishing Group, Nature Reviews Microbiology, 2005 Feb; 3(2):129-43. Copyright © 2005, Rights Managed by Nature Publishing Group. Fig. 1.6: Copyright American Society for Microbiology, Clinical Microbiology Reviews, 1999 Oct; 12(4):633-53. Copyright © 1999, American Society for Microbiology. Fig. 1.8: Copyright Elsevier Inc., Plasmid, 2005 Jan; 53(1):1-13. Epub 2004 Dec 16. Copyright © 2005 Elsevier Inc. Figs. 1.9, 1.10: Copyright American Chemical Society, Biochemistry, 2014 Jul 15; 53(27):4323-33. doi: 10.1021/bi500059y. Epub 2014 Jul 1. Copyright © 2014 American Chemical Society. Fig. 1.12: Copyright Nature Publishing Group, Nature Reviews Microbiology, 2011 Mar; 9(3):153-65. doi: 10.1038/nrmicro2505. Epub 2011 Feb 1. Copyright © 2011, Rights Managed by Nature Publishing Group. CHAPTER TWO: Copyright American Society for Microbiology, Infection and Immunity, 2016 May 24; 84(6):1743-52. doi: 10.1128/IAI.01347-15. Print 2016 Jun. Copyright © 2016, American Society for Microbiology CHAPTER THREE: Copyright John Wiley & Sons Inc., Molecular Microbiology, 2016 July 15; In press. doi: 10.1111/mmi.13463. Copyright © 2016, John Wiley & Sons Inc. Copyrighted materials were used with permission see Appendix MOTILITY AND CHEMOTAXIS IN THE LYME DISEASE SPIROCHETE BORRELIA BURGDORFERI: ROLE IN PATHOGENESIS by Ki Hwan Moon APPROVED BY: DIRECTOR OF DISSERTATION _____________________________ MD A. Motaleb, Ph.D. COMMITTEE MEMBER _____________________________ Everett C. Pesci, Ph.D. COMMITTEE MEMBER _____________________________ R. Martin Roop, II, Ph.D. COMMITTEE MEMBER _____________________________ Shaw M. Akula, Ph.D. COMMITTEE MEMBER _____________________________ Stephanie L. Richards, Ph.D. CHAIR OF THE DEPARTMENT OF MICROBIOLOGY AND IMMUNOLOGY ______________________________ Everett C. Pesci, Ph.D. INTERIM DEAN OF THE GRADUATED SCHOOL ______________________________ Paul J. Gemperline, Ph.D. ACKNOWLEDGEMENTS First and foremost, I offer my sincerest gratitude to my advisor, Dr. MD A. Motaleb, who has supported and guided me throughout the years. The way he mentored me, the knowledge he shared, and the care he took has made me a better person both in the lab and in life. I really appreciate his effort and patience. I would like to thank my collaborators, Drs. Jun Liu and Xiaowei Zhao, in University of Texas in Houston. Without them, these research projects would be incomplete, as they provided the cryo-electron tomogram data. I also thank my committee members, Drs. Everett C. Pesci, R. Martin Roop, II, Shaw M. Akula, and Stephanie L. Richards, who dedicated their time to guide and support me to graduate on time. Moreover, I am grateful to every faculty member in the Department of Microbiology and Immunology who gave me this great opportunity to work and study in the Brody School of Medicine at East Carolina University. I also owe a great deal to my teammates in the Motaleb laboratory. I would like to thank the previous lab Postdocs, Drs. Syed Z. Sultan and Elizabeth A. Novak. Syed helped me with experimental training. His wonderful skills and advice always motivated me. Liz was always ready to lend a hand not only at the bench, but also with my writing. She has been the best Science and English teacher for me. I want to thank the previous lab technician Akarsh Manne and Master student Aaron M. Yerke for being great friends and roommates, who were always ready to help me, in or out of the laboratory. Their cheerful demeanor definitely helped make bench work more enjoyable. I also want to thank the current lab members, Postdoc Dr. Hui Xu, technician Zhou Yu, and Ph.D. student Priyanka A.S. Theophilus for their exuberance and friendly atmosphere. Thanks also to all staff and students in the Biotechology building for providing a great learning environment, and the staff in the Department of Comparative Medicine who helped me with my animal experiments. Additionally, I would like to thank all my friends who I met in US for their friendship. A special thanks goes to Aaron’s family who considered me a part of their own family, and my Brody admission siblings, who made this long journey with me. I appreciate and thank my M.S. advisor and ECU alumnus Dr. Ho Young Kang, and his lab members (my old teammates) who always encouraged me. Dr. Kang initially brought me into the field of bacteriology and introduced me to ECU. Without his guidance and support, I even could not think about studying microbiology abroad. I also want to thank my best friends Deuk Jong Yoo, Kwang Hyun Jeon, Bong Seon Kim, and Young Tae Jeong for their encouragement and support. Thanks also to all my friends in South Korea for their friendship from the halfway across the world, and my friends in US for sharing the empathy as an international student. Lastly, I am immensely grateful to my parents, Mr. Seong Yeor Moon and Mrs. Mi Hee Park who have always been there for me, to strengthen me, and cheering me up. Without their unconditional love, I could not have seen my way through to the completion of this Ph.D. program. I also want to thank my bother Ki Seop Moon, my sister-in-law Ju Myung Moon, and my first nephew Damkong who will be born in November for supporting and encouraging me in this endeavor. Additionally, I would like to thank my grandfather Mr. Byeong Jo Moon who gave tremendous love to his first grandson, and I deeply regret that I could not make to attend his funeral. RIP grandfa! TABLE OF CONTENTS LIST OF TABLES···························································································ix LIST OF FIGURES··························································································x CHAPTER ONE: INTRODUCTION·····································································1
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