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Bacterial Association Networks from Healthy and Cancer- Associated Gut Microbiomes

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Bacterial Association Networks from Healthy and Cancer- Associated Gut Microbiomes University of Central Florida STARS Electronic Theses and Dissertations, 2020- 2021 Bacterial Association Networks from Healthy and Cancer- associated Gut Microbiomes Mark Loftus University of Central Florida Part of the Bacteria Commons, and the Cancer Biology Commons Find similar works at: https://stars.library.ucf.edu/etd2020 University of Central Florida Libraries http://library.ucf.edu This Doctoral Dissertation (Open Access) is brought to you for free and open access by STARS. It has been accepted for inclusion in Electronic Theses and Dissertations, 2020- by an authorized administrator of STARS. For more information, please contact [email protected]. STARS Citation Loftus, Mark, "Bacterial Association Networks from Healthy and Cancer-associated Gut Microbiomes" (2021). Electronic Theses and Dissertations, 2020-. 726. https://stars.library.ucf.edu/etd2020/726 BACTERIAL ASSOCIATION NETWORKS FROM HEALTHY AND CANCER-ASSOCIATED GUT MICROBIOMES by MARK CHRISTIAN LOFTUS B.A. Digital Media, University of Central Florida, 2015 M.S. Biomedical Sciences, University of Central Florida, 2018 A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Burnett School of Biomedical Sciences in the College of Medicine at the University of Central Florida Orlando, Florida Summer Term 2021 Major Professor: Shibu Yooseph © Mark Christian Loftus ii ABSTRACT The human gastrointestinal tract is colonized by a diverse community of symbiotic microorganisms, mainly bacteria, that are known to play essential roles in maintaining the health of their human host. Disruption of this bacterial community has been associated with numerous diseases, including Colorectal Cancer (CRC). CRC is one of the leading causes of cancer-related deaths worldwide. As such, focus has been placed on the modulation of the bacterial community within the cancer-associated gut microbiome as the next step in possible CRC treatment and prevention strategies. To use the bacterial community for these purposes, a better understanding of the associations that exist between bacteria within the healthy human gut microbiome and how these associations have changed within the CRC-associated gut microbiome is direly needed. In this dissertation, we first utilized whole-genome shotgun sequence data from four previously published healthy human cohorts to explore the composition and community structure of the healthy gut microbiome across populations. We show that despite species carriage differences, bacterial communities across healthy human populations are similar in both their structure and functional capacities. In addition, we found that positive associations occur between taxonomically and functionally related species in the gut microbiome. In follow-up work, we employed a similar approach to study the bacterial community composition and structure in late- stage CRC patient gut microbiomes. We found key differences between CRC and healthy gut bacterial communities, suggesting an overgrowth of potentially pathogenic species classified as oral microbes. Additionally, a striking difference in the bacterial community structure was found which we believe to be a bacterial response to probable ecosystem changes associated with iii tumor formation in the CRC-associated gut microbiome. Overall, our findings shed new light on how the bacterial community is structured within the healthy gut microbiome and how this structure has changed in the late-stage CRC-associated gut microbiome. iv To my wife, Kelsey, who has been a continuous source of encouragement and love as I go through the Ph.D. program. You have sacrificed a lot over the years to support me as I follow my dreams. I know that without you, I would not have been able to come this far. I do not know what I have done to deserve a wife as wonderful as you. I love you. To my parents, Shelly, and Paul, Loftus who have never once doubted my abilities and have always pushed me to be the best that I can be. So many times, I came to you tired and upset, and you managed to pick my spirit back up and help me continue forward. You have always been there for me, and I can never repay your unwavering support and love. I am lucky to have you two as my parents. v ACKNOWLEDGMENTS I would like first to acknowledge my long-time mentor Dr. Shibu Yooseph. When I first started the Biomedical Sciences graduate program, I had a Bachelor’s in Digital Media and only a minor in Biology. Many professors had doubts, which they made very clear, concerning my ability to finish the program. Unlike those professors, Dr. Yooseph never made me feel like I could not accomplish my dreams. I cannot state enough that I would not be where I am today without his guidance and patience. I am eternally grateful for the opportunity to learn and work with him. Thank you for all that you have taught me and the gift you have given me. I would also like to acknowledge the members of my dissertation committee, Dr. Anna Forsman, Dr. Taj Azarian, and Dr. Sean Moore. Your critiques and guidance over the years have helped show me how to think like a true researcher. I truly appreciate the time you have sacrificed and the understanding you have shown to me while you have been on my committee. Thank you all. vi TABLE OF CONTENTS LIST OF FIGURES ....................................................................................................................... xi LIST OF TABLES ....................................................................................................................... xiv LIST OF ABBREVIATIONS ....................................................................................................... xv CHAPTER 1: INTRODUCTION ................................................................................................... 1 The Human Gut Microbiome ...................................................................................................... 1 A Brief History of the Human Gut Microbiome Field ...............................................................11 The Gut Microbiome and Colorectal Cancer ............................................................................ 19 Current Cancer Treatments and the Gut Microbiome ............................................................... 29 Bacterial Community Structure ................................................................................................ 36 Dissertation Research Focus and Study Design ........................................................................ 43 CHAPTER 2: BACTERIAL ASSOCIATIONS IN THE HEALTHY HUMAN GUT MICROBIOME ACROSS POPULATIONS ................................................................................ 46 Abstract ..................................................................................................................................... 46 Introduction ............................................................................................................................... 47 Materials and Methods .............................................................................................................. 51 Data Acquisition.................................................................................................................... 51 Data Pre-Processing .............................................................................................................. 54 vii Read Mapping and Species-Level Taxonomic Profiling ...................................................... 56 Bacterial Genome Annotation and Functional Profiles ........................................................ 59 Cohort Sample Functional Profiling ..................................................................................... 60 Random Forest Classifier ...................................................................................................... 61 Construction of Bacterial Association Networks .................................................................. 62 Network Property, Clique, and Module Analysis ................................................................. 63 Network Node Centrality (“Hubs” and “Bottlenecks”) Analysis ......................................... 66 Results ....................................................................................................................................... 67 Signature Species in the Healthy Human Gut Microbiome .................................................. 67 Bacterial Association Networks ............................................................................................ 71 Theoretical Ecology Based on Bacterial Association Networks........................................... 76 Network Cliques and Module Detection............................................................................... 84 Node Centrality Analysis ...................................................................................................... 94 Discussion ................................................................................................................................. 98 CHAPTER 3: BACTERIAL COMMUNITY STRUCTURE ALTERATIONS WITHIN THE COLORECTAL CANCER GUT MICROBIOME ..................................................................... 105 Abstract ................................................................................................................................... 105 Introduction ............................................................................................................................
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