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Evidence for a Direct Link Between the Tol-Pal Protein Complex and Gram Negative Bacteria Cell Division Via an Interaction Between Tolq and the Divisome Protein Ftsn

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Evidence for a Direct Link Between the Tol-Pal Protein Complex and Gram Negative Bacteria Cell Division Via an Interaction Between Tolq and the Divisome Protein Ftsn EVIDENCE FOR A DIRECT LINK BETWEEN THE TOL-PAL PROTEIN COMPLEX AND GRAM NEGATIVE BACTERIA CELL DIVISION VIA AN INTERACTION BETWEEN TOLQ AND THE DIVISOME PROTEIN FTSN Mary A. Teleha A Dissertation Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY August 2013 Committee: Dr. Ray A. Larsen, Advisor Dr. Roudabeh J. Jamasbi Graduate Faculty Representative Dr. Rex L. Lowe Dr. Adam C. Miller Dr. Vipaporn Phuntumart Dr. Scott O. Rogers ii ABSTRACT Ray Larsen, Advisor The TolQ protein functions to couple cytoplasmic membrane-derived energy to support outer membrane processes in Gram negative bacteria. With other products of the widely-conserved tol-pal gene cluster, TolQ has been linked to the process of bacterial cell division. When present in excess, TolQ disrupts cell division, leading to filamentous growth of Escherichia coli. The potential role of TolQ in Gram negative cell division was investigated by a number of methods, including growth assays and immunoblot, two-hybrid, and mutational analyses. This filamentation phenotype is specific for TolQ over-expression independent of TolA and TolR levels, with the degree of filamentation directly proportional to TolQ levels. Over-expression of E. coli TolQ in closely related species indicates that this property of TolQ is not E. coli specific, as excess TolQ leads to a comparable phenotype in other Gram negatives. Bacterial two-hybrid analysis indicates a potential in vivo interaction between TolQ and the divisome protein FtsN, ostensibly one that competitively diverts FtsN from functioning efficiently during late-stage cell division. Filamentation resulting from TolQ over-expression can be suppressed in cells when FtsN is concurrently expressed in excess. Mutational analysis of the 19 amino acid TolQ N- terminus suggests that specific residues within and/or conformation of the extreme N-terminal region of TolQ are essential for filamentation. Results of this study indicate that the link between the Tol-Pal proteins and cell division is mediated in part through a direct interaction between the periplasmic regions of TolQ and FtsN, with a possible role for the Tol system in stabilization of the divisome during Gram negative cell division. These findings are presented in iii this dissertation along with a broader consideration of a role for the Tol-Pal complex in cell division and a dynamic nature for the bacterial cell division apparatus itself. iv ACKNOWLEDGEMENTS I would first like to acknowledge Dr. John Crooks of Lorain County Community College and Dr. Stan Smith of Bowling Green State University for laying the foundation for my graduate programs. While Dr. Crooks has moved on to a new position at LCCC and Dr. Smith passed away while I was at BG, I would not have had this opportunity without the efforts of both. A special thank you to all at BG and LCCC who helped facilitated my program to its end. In particular, I would like to thank Dr. Jeff Miner. To my research advisors, Dr. Ray Larsen and Dr. Adam Miller, I am also appreciative. Thank you, Dr. Larsen, for introducing me to this work and teaching me the research and lab skills to make it my best work, that which I can be proud of. I very much appreciate your willingness to expand the scope of your lab to include the work in this dissertation and your working so hard with me to see this dissertation to completion. To Dr. Miller, thank you for giving so much of yourself to this project and my program. You have been an invaluable teacher and collaborator to me and your support has always meant so much. Without you both, Ray and Adam, I would not be writing this today. I have been so fortunate to have had such an exceptionally supportive and admirable committee. To Dr. Rex Lowe, Dr. Scott Rogers, and Dr. Vipaporn Phuntumart, I thank you each for the kindness, encouragement, and guidance you have given me. I admire and respect so much about each of you, from how you conduct yourselves as fellow scientists to your passions about your work, which each of you have shared so willingly with me. I would also like to offer my sincere appreciation for Dr. Roudabeh Jamasbi. If I were to have chosen for myself, I don’t believe I would have found a more compassionate, supportive, and fair representative for this committee. You are truly a professional with a kind heart. As I leave Bowling Green, it is my v hope that I can take with me the many gifts of character that each of you have shared with me and serve them justice throughout my own professional career. To my family, Mark, Michael, and Kristen, I wish to offer my appreciation and love. Thank you for your support and efforts to encourage me throughout this process. Michael and Kristen, I am so proud of you both for being the best “you” that is possible. To my sister Connie, thank you for always supporting me, always loving me, and always encouraging me. Lastly, to my father, John Simon, thank you for recognizing my hard work and for telling me that you do. As a parent, I think we often feel pride in our children, but sharing that feeling with your child can make a difference when the road becomes bumpy and uncertain, as it did for me. I would like to acknowledge two students who were interested enough in my project to work with me as undergraduates: Brittany Jacob and Donna Ruth. Donna, who has worked with me on this project long enough to develop her own related project, tells me that I inspire her. Donna, you are the one who inspires me. You inspire me to be kinder, more forgiving, stronger, and more determined. You are so much more capable than you think you are. Don’t ever stop asking questions. I would also like to thank Ron Jantz at LCCC for photographing some of my research results, which eventually made it into this dissertation. Lastly, I would like to acknowledge a small group of individuals who have in one way or another become my biggest supporters, my closest friends, and my heroes: Elin LeClaire, Kathryn French, Dave Karohl, Barb Schmittgen, Lysa Styfurak, Katie Hogan, Suzie Moreno, and Chad Braley. Additionally, I would like to acknowledge those individuals at LCCC who were first my teachers so long ago and are now my colleagues and friends. It means so much to me that you believed in me back then, and continue to believe in me today. vi TABLE OF CONTENTS Page CHAPTER I. INTRODUCTION ........................................................................................... 1 Gram Negative Bacteria ........................................................................................... 1 The Tol-Pal Complex ................................................................................................. 5 Gram Negative Cell Division..................................................................................... 16 Research Aims ........................................................................................................... 20 CHAPTER II. CORRELATION BETWEEN ARABINOSE INDUCTION LEVELS AND TOLQ PROTEIN EXPRESSION AMOUNTS AND THE CONSERVED NATURE OF THE TOLQ OVER-EXPRESSION DIVISION PHENOTYPE ................... 23 Introduction ............................................................................................................... 23 Methods ..................................................................................................................... 27 Results ........................................................................................................................ 33 Discussion .................................................................................................................. 44 CHAPTER III. POTENTIAL INTERACTION BETWEEN TOLQ AND FTSN AND THE IMPACT OF THEIR DUAL OVER-EXPRESSION ON DIVISION PHENOTYPE ............................................................................................................ 49 Introduction ............................................................................................................... 49 Methods ..................................................................................................................... 58 Results ........................................................................................................................ 78 Discussion .................................................................................................................. 85 vii CHAPTER IV. THE CONTRIBUTION OF THE N-TERMINAL REGION OF THE TOLQ PROTEIN TO THE OVER-EXPRESSION DIVISION PHENOTYPE AS ANALYZED THROUGH SEQUENCE MODIFICATION ........................................... 89 Introduction ................................................................................................................ 89 Methods ..................................................................................................................... 95 Results ........................................................................................................................ 107 Discussion .................................................................................................................. 127 CHAPTER V. SUMMARY AND GENERAL CONCLUSIONS. ....................................... 138 REFERENCES ...................................................................................................................... 152 APPENDIX A Over-expression of the Escherichia coli TolQ protein leads to a null-FtsN-like division phenotype ........................................................................................
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