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A Population Study of the Upper Airway Microbiota in Busselton, Western Australia

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A Population Study of the Upper Airway Microbiota in Busselton, Western Australia A Population Study of the Upper Airway Microbiota in Busselton, Western Australia ELENA MIROSLAVOVNA TUREK National Heart and Lung Institute, Faculty of Medicine, Imperial College London A Thesis Submitted for the Degree of Doctor of Philosophy ABSTRACT Abstract That the healthy lungs are sterile has been a subject of much debate. Recent studies employing culture independent techniques have focused on investigating the diseased lungs with little still being done to characterise the bacteria which sustain the healthy lung ecosystem. The Busselton Health Study (BHS) is a long running epidemiological study that focuses on defining and characterizing common diseases. Recently addition of oropharyngeal (throat) swabs to the BHS sample collection has occurred. The main aims of this thesis therefore were to assess the upper airway microbiome in healthy individuals and evaluate the changes to the bacterial composition under disease and environmental stress (smoking). A random population sample of 529 participants was studied consisting of 60 current-smokers, 216 ex-smokers and 253 never-smokers, out of which there were 77 asthmatics, 46 subjects with gastro-esophageal reflux disease (GERD), 19 patients with diabetes and 387 healthy individuals. Bacterial DNA was extracted from all swabs and 16S rRNA gene qPCR and next generation sequencing performed. The results indicated that airways of healthy individuals contain a diverse collection of bacteria. Through application of weighted correlation network analysis (WCNA), these bacteria were seen to work together in tight networks. As the BHS cohort is a general population sample no severe disease phenotypes were noted, hence limited changes in bacterial community structure of participants with disease compared to healthy participants were seen. Smoke exposure however had a profound effect on the microbiome, with current- smokers exhibiting a significant drop in bacterial burden, diversity and a change in community structure. There was depletion of Haemophillus spp. and Neisseria spp. in current-smokers, and a strong positive relationship with streptococci. Notably within the first few years after cessation of smoking the bacterial community of the airways appears to regenerate with an increase in community diversity. i ABSTRACT A streptococci specific quantification assay and sequencing method (based on the map gene) was established in order to dissect further the relationship at the species level of the genus Streptococcus with current-smoking. This identified an increased dominance of Streptococcus salivarius (an opportunistic pathogen) in current-smokers. In conclusion, a healthy airway microbiome contains a rich community of microorganisms. This is significantly impacted by smoking, leading to loss of diversity and a community dominated by streptococci. Diversity however can be restored if smoking cessation occurs. ii DECLARATION Declaration of Originality I declare that I completed this thesis, performed all the experiments and data analysis described herein myself, except where appropriately referenced. Elena Turek The copyright of this thesis rests with the author and is made available under a Creative Commons Attribution Non-Commercial No Derivatives licence. Researchers are free to copy, distribute or transmit the thesis on the condition that they attribute it, that they do not use it for commercial purposes and that they do not alter, transform or build upon it. For any reuse or redistribution, researchers must make clear to others the licence terms of this work. iii ACKOWLEDGEMENTS Acknowledgements I would like to begin by thanking my supervisors, Professors Miriam Moffatt and William Cookson. I came to you as a complete novice in everything science related, and with a lot of patience, guidance and support you have moulded me into the person I am today. Someone who has truly suffered my journey through science is Dr Mike Cox and I’m forever grateful. I would like to thank the Busselton team, Professors Bill Musk, Alan James, Matthew Knuiman and Matthew Hunter, who have provided us with this incredible study cohort, and have been very helpful in getting information needed. I would like to thank all the other members of Molgen group past and present that have been there in all my experiences. A special credit goes to Dr Phillip James, who taught me how to google and a lot of R, and who still keeps me on my toes when he’s bored in the lab. I would like to thank Dr Saffron Willis Owen with helping me on the all the network analysis (Chapter 4, WCNA), your knowledge of statistics and coding is inspiring. I would like to thank Dr Huw Christopher Ellis for keeping me sane, and Dr Claire McBrien for undoing Huw’s hard work and making me sign up for a marathon. Finally, I wish to thank all the people that have made the work environment so enjoyable, for their discussions, time and a lot of cake, in particular Leah, Sharon, Giovanna, Verdiana, Colin and Kenny who never fails to deliver. Over the years you have all become my science family. Next, I would like to thank my jitsu family, who have kept me broken and are always there when I needed to blow off steam. Constantinos, you are one of my oldest friends, somehow you managed to pick up the pieces of me and guide them through the brown and black belt gradings. Your faith and belief, powered me to smash through all the obstacles. Imperial Jitsu, who have all been my light at the end of a long day in the lab. Shaan you are probably world’s second-best president (after VVP). Also, Leo, Tilly, Clement, Arnie, Ian B, Alex M, Barry and Neil for being awesome. iv ACKOWLEDGEMENTS I would also like to thank my family. My wonderful husband Dr Vladimir Turek, who is my love, my rock, my soulmate and my best friend. My son Misha, who is my light and the most incredible boy in the world, and with this prepare to have a new bed time story book. My new set of parents (my in-laws) and extended siblings, Yulya, Yura, and especially Tatiana, who have all welcomed me with open arms. Thank you to my wonderful auntie Nadia and sister Catherine. Lastly, a special mention to my best friend, Dr Natalia Yankova, who is like a sister to me. Finally, I would like to dedicate this doctorate thesis to the greatest woman on earth, who single-handedly brought me up; you are the most inspiring, loving, caring mother and now grandmother. You have always taught me to be my very best, pushed me to work harder than humanly possible and that with hard work anything can be achieved. I owe everything I am to you and I thank you, моя мамочка. v TABLE of CONTENTS Table of Contents ABSTRACT .................................................................................................... I DECLARATION OF ORIGINALITY ...................................................................... III ACKNOWLEDGEMENTS ..................................................................................... IV TABLE OF CONTENTS ........................................................................................ VI FIGURES AND TABLES ........................................................................................ X ABBREVIATIONS ............................................................................................. XIII CHAPTER 1 INTRODUCTION ....................................................................... 1 1.1 Background .......................................................................................................................................... 1 1.1.1 The Microbial World ..................................................................................................................................... 1 1.1.2 Sequencing Technology .............................................................................................................................. 3 1.1.3 Bacterial Identification ................................................................................................................................ 3 1.2 Human Microbiome .......................................................................................................................... 5 1.2.1 Overview of the Human Microbiome .................................................................................................... 5 1.2.2 Respiratory System ....................................................................................................................................... 7 1.2.2.1 Healthy Respiratory Microbiome ............................................................................................. 11 1.2.2.2 Asthma ................................................................................................................................................. 12 1.2.2.3 Cigarette Smoke ............................................................................................................................... 14 1.2.2.4 Diabetes ............................................................................................................................................... 15 1.2.2.5 GERD ..................................................................................................................................................... 17 1.2.3 Challenges of Respiratory Microbiome Research ......................................................................... 19 1.3 Busselton Health Study .................................................................................................................. 20 1.4 Thesis Aims .......................................................................................................................................
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