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Microbial and Metabolic Relationships of the Preterm Gut Microbiome in Response to Antibiotic and Dietary Interventions

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Microbial and Metabolic Relationships of the Preterm Gut Microbiome in Response to Antibiotic and Dietary Interventions Microbial and Metabolic Relationships of the Preterm Gut Microbiome in Response to Antibiotic and Dietary Interventions by Sandi Yen A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy In Molecular and Cellular Biology Guelph, Ontario, Canada © Sandi Yen, November 2019 ABSTRACT MICROBIAL AND METABOLIC RELATIONSHIPS OF THE PRETERM GUT MICROBIOME IN RESPONSE TO ANTIBIOTIC AND DIETARY INTERVENTIONS Sandi Yen Advisors: University of Guelph, 2019 Emma Allen-Vercoe Marc G. Aucoin The progression of preterm infant gut microbiome development is intricately linked with the development of the infant, such that disruptions to the microbial system can manifest as neonatal necrotizing enterocolitis (NEC) in the infant. One of the proposed aetiologies of NEC is that disease onset occurs when microbiome development is challenged by an external perturbation, such as antibiotic treatment. The research conducted in this thesis was motivated by the overarching hypothesis that infant health occurs when homeostatic microbial relationships have been established. Conversely, when microbiome development is disrupted, the preterm infant is susceptible to diseases such as NEC. Therefore, the driving hypothesis of this thesis was that external factors, such as antibiotic therapy or formula milk, impair microbial interactions such that the preterm gut microbiome no longer sustains healthy infant development, leading to NEC onset. This hypothesis was tested using fecal microbiota from two preterm infants with different antibiotic exposures while in hospital. Propagation of these preterm fecal microbiota in an in vitro continuous culture system allowed for compositional, metabonomic, culture-based annotation of the ecosystems. Longitudinal analysis of each community revealed differences in each community’s functional capacity. The Infant 1 community, which was antibiotic-naïve, was able to restore that same steady-state by 1-2 weeks after antibiotic treatment ended. In contrast, the Infant 2 community (had prior exposure to antibiotics) was not able to re-gain the same compositional state after antibiotic treatment, nor was it able to carry out similar secondary metabolisms. The differences in the two community’s resilience to in vitro antibiotic treatment was attributed to the microbial-microbial relationships in the in vitro communities. This work demonstrated that parenteral antibiotic therapy has the potential to disrupt microbe-microbe relationships such that the microbiome is hindered in its ability to function as a cohesive ecosystem. This work, which includes several other studies focused on examining the metabolic capacity of the early gut microbiome, provides groundwork that potentiates development of therapy alternatives that target endogenous microbial relationships to steer the preterm gut ecosystem towards a state of health. iii DEDICATION This thesis is dedicated to Nicholas Menzies, who has carried me through to the finish line. iv ACKNOWLEDGEMENTS This body of work would be incomplete without the support and contributions of many, many people: Mentorship and guidance from my supervisors: Dr. Emma Allen-Vercoe and Dr. Marc G. Aucoin Support from my advisory committee: Dr. Cezar Khursigara and Dr. Hermann Eberl Strong partnership with collaborators: Dr. Erika Claud, Dr. Prameet Sheth, Dr. Lars Bode, Dr. Jacque Belik Mentorship from NMR wizard: Sameer Al-Abdul-Wahid Advisement from Genomics Guru: Jeff Gross Scientific and personal growth from peer mentors: Dr. Kaitlyn Oliphant, Dr. Rafael José Marques Peixoto, Dr. Christian Carlucci, Dr. Stanislav Sokolenko Collaboration and friendship of colleagues and peers: Erin Shackleton, Alex Pritchard-Oh, Greg Higgins, Charley Carriero, Michelle Daigneault, Chris Ambrose, Dr. Kyla Chochrane, Dr. Kathleen Schroeter, Dr. Julie McDonald, Caroline Ganobis, Simone Renwick, Avery Robertson, Jacob Wilde, Connor Gianetto-Hill, Dr. Claire Watkins, Erin Bolte, AJ Stirling, Keith Sheriff, Joseph Ciufo, Karen Gonzalez, Alyssa Koch, Craig Moore Ineffable support from family: Dad, Mom, Danny, Judy, Anita; Craig, Terry, Justin, Samantha, Jackie, Theo Dedication and trust from: NICU staff, nurses, doctors, parents, and infants at the Comer Children’s Hospital, Kingston General Hospital, Toronto SickKids Hospital v TABLE OF CONTENTS Abstract....................................................................................................................................... ii Dedication .................................................................................................................................. iv Acknowledgements ..................................................................................................................... v Table of Contents ....................................................................................................................... vi List of Tables ............................................................................................................................. xi List of Figures ........................................................................................................................... xii List of Supplementary Tables ................................................................................................... xiv List of Supplementary Figures ................................................................................................... xv List of Supplementary Equations .............................................................................................. xvi List of Abbreviations ................................................................................................................ xvii 1 Literature Review ............................................................................................................... 1 1.1 Introduction .................................................................................................................. 1 1.2 Investigating Microbial Composition with 16S rRNA Gene Sequencing........................ 2 1.2.1 Taxonomic Limitations of 16S rRNA Gene ............................................................ 2 1.3 Preterm Infant Gut Microbiome .................................................................................... 3 1.4 Neonatal Necrotizing Enterocolitis ............................................................................... 6 1.4.1 Risk Factors and Pathogenesis of NEC ................................................................ 6 1.4.2 Antibiotics and NEC .............................................................................................. 8 1.4.3 NEC and the Early Gut Microbiome ...................................................................... 9 1.4.4 Host and Microbial Metabonome during NEC ......................................................10 1.4.5 Feeding Strategies and NEC ...............................................................................12 1.5 Breast Milk Composition and Benefits .........................................................................13 1.5.1 Human Milk Oligosaccharides ..............................................................................14 1.5.2 HMO Metabolism and Distribution ........................................................................20 1.5.3 Biofunctions of HMOs ..........................................................................................22 1.5.4 HMOs and NEC ...................................................................................................24 1.5.5 HMOs Modulate the Gut Microbiota .....................................................................25 1.5.6 HMOs in Infant Formula Milk ................................................................................26 1.6 Project Overview .........................................................................................................27 1.6.1 Global Hypothesis ................................................................................................27 1.6.2 Bioinformatic Workflow for 16S rRNA gene Analysis ............................................28 1.6.3 Antibiotic Detection in Preterm Infant Stool ..........................................................28 1.6.4 Evaluation of Community Resilience to In vitro Antibiotic Treatment ....................29 vi 1.6.5 HMOs as a Substrate for Microbes Derived from Preterm Infant Stool .................30 1.6.6 Contribution to Early Gut Microbiome Research ..................................................30 2 Employing ASV Denoising Balances Bioinformatic and Biological Resolution Using the seqpipeR Workflow ...................................................................................................................32 2.1 Chapter Objective .......................................................................................................32 2.2 Manuscript Authorship ................................................................................................33 2.3 Abstract ......................................................................................................................33 2.4 Introduction .................................................................................................................35 2.4.1 Current State of 16S rRNA Gene Marker Analysis in Microbiome Research ........35 2.4.2 Taxonomic Limitations of 16S rRNA Gene ...........................................................38 2.4.3 Currently Available
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