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A Conserved Inner Membrane Protein of Aggregatibacter Actinomycetemcomitans Is Integral for Membrane Function Kenneth Smith University of Vermont

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A Conserved Inner Membrane Protein of Aggregatibacter Actinomycetemcomitans Is Integral for Membrane Function Kenneth Smith University of Vermont University of Vermont ScholarWorks @ UVM Graduate College Dissertations and Theses Dissertations and Theses 2015 A conserved Inner Membrane Protein of Aggregatibacter actinomycetemcomitans is integral for membrane function Kenneth Smith University of Vermont Follow this and additional works at: https://scholarworks.uvm.edu/graddis Part of the Microbiology Commons Recommended Citation Smith, Kenneth, "A conserved Inner Membrane Protein of Aggregatibacter actinomycetemcomitans is integral for membrane function" (2015). Graduate College Dissertations and Theses. 417. https://scholarworks.uvm.edu/graddis/417 This Dissertation is brought to you for free and open access by the Dissertations and Theses at ScholarWorks @ UVM. It has been accepted for inclusion in Graduate College Dissertations and Theses by an authorized administrator of ScholarWorks @ UVM. For more information, please contact [email protected]. A CONSERVED INNER MEMBRANE PROTEIN OF AGGREGATIBACTER ACTINOMYCETEMCOMITANS IS INTEGRAL FOR MEMBRANE FUNCTION A Dissertation Presented by Kenneth P. Smith to The Faculty of the Graduate College of The University of Vermont In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Specializing in Microbiology and Molecular Genetics October, 2015 Defense Date: June 15, 2015 Dissertation Examination Committee: Keith P. Mintz, Ph.D., Advisor Teresa Ruiz, Ph.D., Chairperson John M. Burke, Ph.D. Aimee Shen, Ph.D. Matthew J. Wargo, Ph.D. Cynthia J. Forehand, Ph.D., Dean of the Graduate College ABSTRACT The cell envelope of Aggregatibacter actinomycetemcomitans, a Gram-negative pathogenic bacterium implicated in human oral and systemic disease, plays a critical role in maintenance of cellular homeostasis, resistance to external stress, and host–pathogen interactions. Our laboratory has identified a novel gene product, morphogenesis protein C (MorC), deletion of which leads to multiple pleotropic effects pertaining to membrane structure and function. The MorC sequence was determined to be conserved in Gammaproteobacteria. Based on this bioinformatic analysis, the functional conservation of this protein was investigated utilizing an A. actinomycetemcomitans morC mutant as a model system to express homologs from four phylogenetically diverse representatives of the Gammaproteobacteria: Haemophilus influenzae, Escherichia coli, Pseudomonas aeruginosa, and Moraxella catarrhalis. MorC from all organisms restored at least one of the A. actinomycetemcomitans mutant phenotypes, implying that the protein is functionally conserved across Gammaproteobacteria. Further, deletion mutagenesis indicated that the last 10 amino acids of the carboxyl terminus were necessary to maintain the integrity of the membrane. The observed pleiotropic effects suggested alterations in the membrane protein composition of the morC mutant. Stable isotope dimethyl labeling in conjunction with mass spectrometry was employed to quantitatively determine the differences in the abundance of membrane proteins of the isogenic mutant and wild-type strains. A total of 665 envelope associated proteins were identified and functionally annotated using bioinformatic tools. All proteins, except MorC, were detected in the mutant strain. However, 12 proteins were found in lesser (10) or greater (2) abundance in the membrane preparation of the mutant strain. These proteins were ascribed functions associated with protein quality control, oxidative stress response, and protein secretion systems. One protein found to be reduced was a component of the fimbrial secretion system of A. actinomycetemcomitans. The significance of this finding was unclear due to the afimbriated nature of the laboratory strain used in the study. Therefore, the defect in fimbriation was identified and complemented in trans. The transformed strain displayed all of the hallmarks of a naturally fimbriated strain including: a distinct star-like colony morphology; robust biofilm formation; and presence of fimbriae as detected by electron microscopy. The isogenic morC mutant strain transformed with an identical plasmid did not display any fimbriated phenotypes. The role of MorC in fimbriae production of a naturally fimbriated strain was investigated by inactivation of morC in a clinical isolate. The mutant strain displayed phenotypes typically associated with inactivation of morC. However, fimbriae were still observed on the surface, although in lesser amounts on some individual bacteria, and this strain formed a biofilm with volume similar to the parent. Interestingly, significant changes in microcolony architecture of the biofilm were observed by confocal microscopy. MorC plays a critical role in maintaining secretion of major virulence determinants of A. actinomycetemcomitans. Specific changes in the protein composition of the cell envelope indicate a direct or compensatory role of these proteins in maintaining membrane physiology. The functional conservation of MorC also implies an important role for this protein in other Gram-negative bacteria. This work suggests a role of MorC as an accessory or a scaffold protein involved in secretion. CITATIONS Material from Chapter 2 of this dissertation has been submitted for publication to Molecular Oral Microbiology in June 2015 in the following form: Smith, K.P., Voogt, R.D., Ruiz, T., and Mintz, K.P.. The conserved carboxyl domain of MorC, an inner membrane protein of Aggregatibacter actinomycetemcomitans, is essential for membrane function. Material from Chapter 3 of this dissertation has been published in the following form: Smith, K. P., Fields, J. G., Voogt, R. D., Deng, B., Lam, Y, and Mintz, K.P.. (2014) The cell envelope proteome of Aggregatibacter actinomycetemcomitans. Molecular Oral Microbiology. DOI: 10.1111/omi.12074 Material from Chapter 4 of this dissertation has been accepted for publication in the following form: Smith, K. P., Fields, J. G., Voogt, R. D., Deng, B., Lam, Y, and Mintz, K.P.. (2015) Alteration in abundance of specific membrane proteins of Aggregatibacter actinomycetemcomitans is attributed to deletion of the inner membrane protein MorC. Proteomics. In press. Material from Chapter 5 of this dissertation has been submitted for publication to Journal of Bacteriology in the following form: Smith, K.P., Ruiz, T., and Mintz, K.P.. The Inner Membrane Protein, MorC, is involved in fimbriae production and biofilm formation in Aggregatibacter actinomycetemcomitans. ii ACKNOWLEDGEMENTS First, I would like to thank my mentor, Keith Mintz. His patience and tenacity when faced with difficult problems consistently inspired me and will continue to do so throughout my career. I was always able to speak freely and candidly with Keith and our conversations taught me a great deal about the practical aspects and philosophical underpinnings of conducting research. His understanding nature combined with his professional and personal guidance was integral to my success. I look forward to our continued discussion and collaboration. I am also thankful for the input and suggestions of my dissertation committee: John Burke, Aimee Shen, and Matt Wargo. I am especially grateful to Teresa Ruiz, my committee chair and close collaborator. Her expertise in the field of electron microscopy is unmatched and it was a privilege to learn from her. Teresa was also very supportive and our many discussions improved not only my dissertation but also my skills as a scientist. In addition to my mentors at the University of Vermont, I would also like to thank Manuel Varela, my master’s thesis advisor at Eastern New Mexico University. I am indebted to him for helping me start my career in microbiology and for teaching me the fundamental aspects of doing research. Richard Voogt, research technician in the Mintz laboratory, was a great friend and colleague throughout my time as a graduate student. Xuan Jiang, a previous graduate student in the laboratory, helped me make the transition to the University of Vermont and provided friendship and valuable advice. The unwavering support of Richard and Xuan was greatly appreciated. I am also grateful for my friendship with other members of the iii laboratory including David Danforth, Thomas Freeman, and Yan Xing, all of whom contributed significantly to the success of my research. I would also like to acknowledge my colleague Jenna Foderaro. My friendship with Jenna began early on in the program and our discussions about classes, research, and life in general made my time at the University more enjoyable. I am thankful that she has always been there to help me when I needed it most and look forward to our continuing friendship. My parents Kenneth and Debra Smith have also played an extremely important role in my educational career. They are tireless in their support and have always gone above and beyond to help me in any way that they can throughout my time as a student. Their assistance in both practical and personal matters truly made this dissertation possible and I will always look up to them as examples. iv TABLE OF CONTENTS Citations ...........................................................................................................................ii Acknowledgements ..........................................................................................................iii List of Tables ...................................................................................................................ix List of Figures ..................................................................................................................x
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