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Aerococcus Urinae: Establishing the Pathogenesis of an Emerging Uropathogen

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Aerococcus Urinae: Establishing the Pathogenesis of an Emerging Uropathogen Loyola University Chicago Loyola eCommons Dissertations Theses and Dissertations 2019 Aerococcus Urinae: Establishing the Pathogenesis of an Emerging Uropathogen Evann E. Hilt Follow this and additional works at: https://ecommons.luc.edu/luc_diss Part of the Microbiology Commons Recommended Citation Hilt, Evann E., "Aerococcus Urinae: Establishing the Pathogenesis of an Emerging Uropathogen" (2019). Dissertations. 3339. https://ecommons.luc.edu/luc_diss/3339 This Dissertation is brought to you for free and open access by the Theses and Dissertations at Loyola eCommons. It has been accepted for inclusion in Dissertations by an authorized administrator of Loyola eCommons. For more information, please contact [email protected]. This work is licensed under a Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 License. Copyright © 2019 Evann E Hilt LOYOLA UNIVERSITY CHICAGO AEROCOCCUS URINAE: ESTABLISHING THE PATHOGENESIS OF AN EMERGING UROPATHOGEN A DISSERTATION SUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOL IN CANDIDACY FOR THE DEGREE OF DOCTOR OF PHILOSOPHY PROGRAM IN MICROBIOLOGY AND IMMUNOLOGY BY EVANN ELIZABETH HILT CHICAGO, ILLINOIS AUGUST 2019 Copyright by Evann Elizabeth Hilt, 2019 All rights reserved. ACKNOWLEDGEMENTS I would like to thank everyone that made this dissertation. First and foremost, I want to thank my mentor, Alan Wolfe. I couldn’t ask for a better mentor throughout both my masters and PhD. He created a very supportive environment in his lab and I am definitely going to miss it. I’d also like to thank the members of my dissertation committee. My committee chair Francis Alonzo for keeping our meetings moving along and asking very insightful questions. To Karen Visick and Phong Le, thank you for being co-mentors in this project and spending endless hours trying to make sense of this work. Finally, Michael Federle, for bringing in an outside persepective and way of thinking to this project. I want to thank my fellow Wolfe lab members past and present. Specifically, I want to thank Krystal Thomas-White and Travis Price for being there by my side as we helped to create the foundation of urinary microbiome research. None of this work would be possible without Meghan Pearce, who laid the foundation for the microbiome projects, Roberto Limeira, who’s skills and overall commitment to the lab were vital, and Thomas Halverson, who’s hard-work and dedication has helped more than you can realize. I want to thank all of the other lab members that I had the pleasure of working with: Linda Hu, Bob Davis, Dave Christiansen, Bozena Zemaitaitis, Giuseppe Pistone, Danielle Johansen, Katie Diebel, Cesar Montelongo-Hernandez, Michelle Van Kuiken-Johnson, Petar Bajic, Ryan Dornbier, Baylie Hochstedler, Sarah Fied and Omar Abdel-Rahim. You have all helped to make this stressful time way more enjoyable. I also want to thank the entire Loyola Education and Research Collaborative (LUEREC) iii My experience “growing up translational” with this group has provided a scaffold of how I want to run a lab and collaborations in the future. I want to thank the current and former urogynecology and urology professors for their leadership, knowledge, and commitment and in particular, Linda Brubaker for your clinical knowledge and passion for the research. I also want to thank all of the urogynecology fellows who have helped work side-by-side with us graduate students in making sure all the studies run smoothly. Lastly, I want to thank Mary Tulke, who easily does the work of three people and still finds time to help me whenever I need it. I also want to thank the entire clinical microbiology team past and present. In particular, I want to thank Violet Rekasius, Joyce Tjhio, and Kathleen McKinley. Working with you all side- by-side and seeing your passion for the field of clinical microbiology has had such a strong influence on my life and my career choices. Thank you for always being there to help or have a quick chat. I want to specially thank Paul Schreckenberger. Your passion for clinical microbiology will always be an inspiration to me. I’d also like to extend my gratitude and thank to all of my friends and family. Having all of your support through this journey has meant the world to me. Specifically to my parents, for always pushing me and being there for me in times of happiness and sadness. I wouldn’t be the woman I am today without their love and support. But none of this would be possible if I didn’t have my husband, Nic. His unconditional love and support is what has gotten me through this experience. He was always there to remind me why I was doing this and I cannot thank him enough for that. iv I dedicate this work to my Grandpa Richard Nielsen. I finally have a book ready for signing at bookstores. TABLE OF CONTENTS ACKNOWLEDGEMENTS iii LIST OF TABLES x LIST OF FIGURES xii LIST OF ABBREVIATIONS xv ABSTRACT xxi CHAPTER ONE: INTRODUCTION AND LITERATURE REVIEW 1 Urinary Tract and Urinary Tract Infections 1 Pathogenesis of Classic Uropathogen 4 Adherence and Colonization 6 Evasion of the Innate Immune Response 7 Persistence 12 History of the “Urine is Sterile” Dogma 15 History of Clinical Microbiology Urine Culture 16 Discover of the Urinary Microbiota/Microbiome 17 Relation of Urinary Microbiome to Lower Urinary Tract Diseases and Disorders 21 How the Urinary Microbiome is Changing the View of Urinary Tract Infections 23 Emerging Uropathogens 25 Aerococcus urinae 28 Aerococcus Infection of Lobsters 29 Aerococcus and Urinary Tract Infections 30 Aerococcus and Invasive Infections 34 Aerococcus and Other Lower Urinary Tract Disorders 37 Summary of Aerococcus 39 Lesson in Genetics (Reverse vs Forward Genetics) 39 Summary of Introduction 41 CHAPTER TWO: METHODS AND MATERIALS 43 Isolation of Clinical Isolates 43 Patients and Sample Collection 43 Standard Urine Culture 43 Expanded Quantitative Urine Culture (EQUC) 44 Identification of Pure Isolates 45 MALDI Data Analyses 45 Storage of Clinical Isolates 46 Growth of Clinical Isolates 46 vi Aerococcus Isolates 46 Lactobacillus Isolates 47 UPEC and Urinary E. coli Isolates 47 Streptococcus Isolates 48 Growth Curves 48 Biofilm Assay 48 Autoinducer Assay 50 Spot Characterization Assay 51 Chemical Mutagenesis Assays 51 Ethylmethanesulfonate (EMS) Treatments 51 ICR-101 Treatments 52 2-Aminopurine (2-AP) Treatments 53 Whole Genome Sequencing of Aerococcus Isolates 53 DNA Extraction 53 Genome Sequencing, Assembly and Annotation 54 Mutant Alignment Analysis 54 Phylogenetic Analysis 55 Functional Genomic Assay 55 Treatment of Urothelial Cell Assays 56 Adherence/Invasion Assay 56 Cytotoxicity Assay 57 Cytokine Bead Array 59 Measurement of TLR Expression 60 Statistical Analyses 61 CHAPTER THREE: EXPERIMENTAL RESULTS 62 Description of Aerococcus urinae Clinical Isolates 62 Growth Characteristics of A. urinae in vitro 78 The ‘Hockey Puck’ Phenotype 93 The ‘Flocking’ Phenotype 95 The ‘Pigmentation’ Phenotype 97 Biofilm Formation 102 Summary 104 Whole Genome Sequencing Comparison of Clinical Isolates to Determine Genes Responsible for the Flocking Phenotype 106 Selection of Clinical Isolates to Sequence 106 Genomic Diversity Amongst A. urinae Strains 108 Examination of Functionally Encoded Coding Regions within the A. urinae genomes 108 Summary 117 Interaction of A. urinae with Human Urothelial Cells (HUCs) 118 Adherence of A. urinae to HUCs 118 Cytotoxicity to HUCs 119 Immune Response of Human Urothelial Cells to Aerococcus urinae 125 Cytokine Production 125 vii TLR Expression 129 Summary 133 Forward Genetics Approach to Determine Genotype of Black Pigmentation Phenotype 134 Ethylmethansulfonate (EMS) Mutagenesis Results 134 ICR-191 Mutagenesis Results 144 Sequence and Alignment of Mutant Genomes 145 Revertant Analysis 147 2-aminopurine Mutagenesis 147 Natural Revertants 148 Confirmation of VW Mutant Phenotypes 149 CHAPTER FOUR: DISCUSSION 151 Introduction 151 Implications and Discussion 152 Future Directions 159 Roles of Auxin Biosynthesis and β-Glucoside Metabolism in ‘Flocking’ Phenotype 160 Completion of VW Mutant Analysis 161 Making A. urinae a Genetically Tractable Organism 162 Bioinformatics Homolog Approach 163 Investigation of Sugar Signals for Biofilm-like Phenotypes 164 A. urinae and Innate Immune Response in HUCs 165 A. urinae and Neurotransmitter Pathways in HUCs 166 Conclusion 168 APPENDIX A: INTRODUCTION TO THE APPENDICES: ADDITIONAL RESEARCH 169 APPENDIX B: THE FEMALE URINARY MICROBIOME: A COMPARISON WITH AND WITHOUT URGENCY URINARY INCONTINENCE 171 APPENDIX C: THE INTERACTION BETWEEN ENTEROBACTERIACEAE AND CALCIUM OXALATE DEPOSITS 204 APPENDIX D: INCONTINENCE MEDICATION RESPONSE RELATES TO THE FEMALE URINARY MICORBIOME 231 APPENDIX E: GENOMES OF GARDNERELLA STRAINS REVEAL AN ABUNDANCE OF PROPHAGES WITHIN THE BLADDER MICROBIOME 263 APPENDIX F: THE CLINICAL URINE CULTURE: ENHANCED TECHNIQUES IMPROVE DETECTION OF CLINICALLY RELEVANT MICROORGANISMS 290 APPENDIX G: URINARY SYMPTOMS AND THEIR ASSOCIATION WITH URINARY TRACT INFECTIONS IN UROGYNECOLOGIC PATIENTS 314 viii APPENDIX H: URINE TROUBLE: SHOULD WE THINK DIFFERENTLY ABOUT UTI? 328 APPENDIX I: PROPOSAL OF ONGOING CLINICAL TRIAL 342 APPENDIX J: MICROORGANISMS IDENTIFIED IN THE MATERNAL BLADDER: DISCOVERY OF THE MATERNAL BLADDER MICROBIOTA 351 APPENDIX K: CULTURING OF FEMALE BLADDER BACTERIA REVEALS AN INTERCONNECTED UROGENITAL MICROBIOTA 370 APPENDIX L: WHOLE GENOME SEQUENCING ANNOUCEMENTS 393 APPENDIX M: FEMALE LOWER URINARY TRACT MICROBTIOA DO NOT ASSOCIATE WITH IC/PBS SYMPTOMS: A CASE-CONTROLLED STUDY 414 APPENDIX N: MIRABEGRON AND URINARY URGENCY INCONTINENCE: THE CLINICAL RESPONSE AND THE FEMALE URINARY MICROBIOME 431 APPENDIX O: ATTEMPTS AT INTROCUTION OF DNA INTO AEROCOCCUS URINAE 451 APPENDIX P: AUTOINDUCER EXPERIMENT 460 APPENDIX Q: R SCRIPTS 464 REFERENCE LIST 468 VITA 534 ix LIST OF TABLES Table 1. Conditions predisposing an individual to UTI 2 Table 2. Guidelines for Empiric Antibiotic Treatment for Uncomplicated UTIs 3 Table 3. Function of Pro-Inflammatory Cytokines in the Urothelium 11 Table 4. Summary of activity of common UTI antimicrobial agents against “Emerging Uropathogens” 26 Table 5. Summary of UTI Studies with ALO/A. urinae 33 Table 6. Summary of activity of common UTI antimicrobial agents against A.
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