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Assessing the Temporal Dynamics of the Lower Urinary Tract Microbiota and the Effects of Lifestyle Loyola University Chicago Loyola eCommons Dissertations Theses and Dissertations 2019 Assessing the Temporal Dynamics of the Lower Urinary Tract Microbiota and the Effects of Lifestyle Travis Kyle Price Follow this and additional works at: https://ecommons.luc.edu/luc_diss Part of the Microbiology Commons Recommended Citation Price, Travis Kyle, "Assessing the Temporal Dynamics of the Lower Urinary Tract Microbiota and the Effects of Lifestyle" (2019). Dissertations. 3367. https://ecommons.luc.edu/luc_diss/3367 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 Travis Kyle Price LOYOLA UNIVERSITY CHICAGO ASSESSING THE TEMPORAL DYNAMICS OF THE LOWER URINARY TRACT MICROBIOTA AND THE EFFECTS OF LIFESTYLE 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 TRAVIS KYLE PRICE CHICAGO, IL MAY 2019 i Copyright by Travis Kyle Price, 2019 All Rights Reserved ii ACKNOWLEDGMENTS I would like to thank everyone that made this thesis possible. First and foremost, I want to thank Dr. Alan Wolfe. I could not have asked for a better mentor. I don’t think there will ever be another period of my life where I grow as a scientist, as a professional, or as a person more than I did under your mentorship. I am forever grateful for that. I want to thank my committee members. My committee chair, Dr. Katherine Knight, for always pushing me to achieve my best and helping shape me into the professional scientist that I am now. Dr. Karen Visick, for always providing insightful comments and thinking and caring about my research as if it was your own. Dr. Qunfeng Dong, for your vast knowledge of bioinformatics and your wonderful input on the research. Dr. Amanda Harrington, for providing the vital perspective of a clinical microbiologist on my work and going out of your way to help me with career aspirations. And to Dr. Elizabeth Mueller, for your amazing leadership of your clinical team, without which, none of this would be possible, and for somehow always finding the time to help me in any way that you could. I want to thank all of my fellow lab members throughout my time in the lab, particularly Evann Hilt and Dr. Krystal Thomas-White; what we accomplished together was incredible. I will always compare my co-workers to your level of excellence. And I am incredibly excited to continue my career journey with Evann at UCLA. None of this work would be possible without Dr. 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, whose hard-work iii 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: Dr. Bob Davis, Dr. Dave Christiansen, Bozena Zemaitaitis, Giuseppe Pistone, Danielle Johansen, Katie Diebel, Cesar Montelongo-Hernandez, Dr. Michelle Van Kuiken-Johnson, Dr. Petar Bajic, Dr. Ryan Dornbier, Baylie Hochstedler, Sarah Fied, Nancy Sloan, Omar Abdel-Rahim, Brian Choi, Michael Bochert, Tom Bank, and Dr. Vibha Ahuja. You all helped make a stressful time in my life easier and more enjoyable. I also want to thank the entire Loyola Education and Research Collaborative (LUEREC). In the future, I will undoubtably compare every team that I work with to LUEREC, and I doubt that I will ever find a more talented, dedicated, and all-around enjoyable team of team of people to work with. From our amazingly productive meetings, to our amazingly entertaining karaoke at AUGS each year, it has truly been a memorable experience. Specifically, I want to thank the wonderful urogynecology fellows that I had the pleasure of working with including Dr. Susanne Taege, Dr. Megan Shannon, Dr. Brandon Chen, and in particular Dr. Tanaka Dune for your hard- work and great collaboration. I also want to individually thank Dr. Birte Wolff. We put in so much time and effort into the studies detailed in this thesis. You made what should have been a very stressful process into a fun and productive one. I want to thank the current and former urogynecology and urology professors for their leadership, knowledge, and commitment: Dr. Cynthia Brincat, Dr. Larissa Bresler, Dr. Colleen Fitzgerald, and Dr. Thythy Pham. In particular, Dr. Linda Brubaker for your clinical knowledge and passion for the research. 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. iv I want to thank Dr. Catherine Putonti and her unbelievably hard-working lab. The collaboration with your lab has been incredibly productive and I personally want to thank you, Carine Mores, and Dr. Jason Shapiro for all your help with the genomic analyses in this thesis. I also want to thank the entire clinical microbiology team past and present. In particular Violet Rekasius, Joyce Tjhio, Kathy McKinley, and Sharon Desjarlais. Working with you all 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 D. Paul Schreckenberger. You had an amazing ability to make anyone feel confident in themselves. Your passion for clinical microbiology will always be an inspiration to me. I wish that the time I knew you could have been much longer. Finally, I would like to thank my friends and family for all of their support. In particular, Jon for sticking by my side during one of the most stressful and demanding periods of my life. v TABLE OF CONTENTS ACKNOWLEDGMENTS iii LIST OF TABLES x LIST OF FIGURES xiii LIST OF ABBREVIATIONS xvi ABSTRACT xix CHAPTER I: INTRODUCTION AND LITERATURE REVIEW 1 The Human Microbiota 1 The Role of the Human Microbiota 2 Measuring the Microbiome 3 Analyzing Microbiome Data 5 “Urine Denial”: The Concept of Bladder Sterility 7 The Discovery of the Female Urinary Microbiota and Microbiome 9 Urine is Not Sterile: Now What? 13 Correlations with Health and Disease 16 Description of Urinary Bacterial Isolates 21 Other Urinary Microorganisms 25 Description of the Male Urinary Microbiota 25 Correlations with Health and Disease 28 Correlations with Lifestyle and Preliminary Measures of Stability 30 Differences between the Male and Female Urinary Microbiota 31 The Microbiome is Shaped by Environment 31 The GI Microbiota and Lifestyle 33 Description of GI Tract Physiology 33 Correlations between the GI Microbiota and Lifestyle 34 Temporal Dynamics of the GI Microbiota 36 The Vaginal Microbiota and Lifestyle 39 Description of Vaginal Tract Physiology 39 Correlations between the Vaginal Microbiota, BV Risk, and Lifestyle 40 Temporal Dynamics of the Vaginal Microbiota 41 UTI Risk and Lifestyle 44 Current Understanding of UTI and an Overview of Risk Factors 44 vi Probiotics and UTI Risk 45 Correlations between UTI Risk and Lifestyle 47 Correlations between UTI Risk and Urine Properties 53 Longitudinal Assessment of the Lower Urinary Tract Microbiota 54 Rational and Problems 55 What Specimen to Collect? 56 Preliminary Findings 63 Summary 64 CHAPTER II: MATERIALS AND METHODS 67 Overview of Clinical Studies 67 MAGnUM Study 68 ProFUM Study 70 PARTNER Study 76 Bacterial Identification Methods 80 Specimen Collection 80 Expanded Culture Protocol 81 16S Sequencing Protocol 82 Dipstick Urinalysis 85 Storage of Bacterial Isolates 85 Statistical Analyses 85 Whole Genome Sequencing 86 DNA Extraction and Library Prep 86 Assembly and Annotation 87 Bacterial Assays: Experimental Procedures 88 Bacterial Strains and Growth Conditions 88 Urothelial Cell Adherence Assays 93 Biofilm Assays 94 Growth Competition Assays 95 CHAPTER III: FEASIBILITY PROJECT: MAGnUM STUDY 96 Overview of MAGnUM Study 96 Longitudinal Assessment of the Microbiota of the Male LUT 96 Longitudinal Assessment of the Microbiota of the Female LUT 100 Summary 106 CHAPTER IV: EFFECT OF INTRINSIC LIFESTYLE FACTORS ON LUT MICROBIOTA 109 Overview of ProFUM Study 109 Screening Eligible Participants 109 vii ProFUM Specimen Integrity 112 Qualitative Description of the Longitudinal LUT Microbiota and Microbiome 115 Measuring the Overall Stability of the LUT Microbiota 122 Menstruation and LUT Microbiota Variability 125 Urine Properties and Constituents and LUT Microbiota Variability 138 Summary 143 CHAPTER V: EFFECT OF EXTRINSIC LIFESTYLE FACTORS ON LUT MICROBIOTA 147 Sexual Activity and LUT Microbiota Variability 147 Hygiene and LUT Microbiota Variability 159 Oral Probiotics and LUT Microbiota Variability 163 Summary 165 CHAPTER VI: MECHANISTIC DETERMINATION AND SIGNIFICANCE OF LUT MICROBIOTA VARIABILITY AND VAGINAL INTERCOURSE 168 Introduction and Rationale 168 Assessing the Clinical Significance of LUT Microbiota Variability Following Vaginal Intercourse 170 Effect of Urinary Isolates on UPEC Adherence to Urothelial Cells 170 Effect of Urinary Isolates on UPEC Biofilm Formation 172 Effect of Urinary Isolates on UPEC Growth 175 Assessing the Ability of Urinary Isolates to Adhere to Urothelial Cells 181 Assessing the Biological Significance of LUT Microbiota Variability Following Vaginal Intercourse 183 Overview of PARTNER
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