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Towards Understanding the Pathobiology of Brachyspira

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Towards Understanding the Pathobiology of Brachyspira Understanding the pathobiology of Brachyspira pilosicoli in order to develop novel intervention strategies against avian intestinal spirochaetosis A thesis submitted by Luke John Mappley For the degree of Doctor of Philosophy 2012 Department of Bacteriology Animal Health and Veterinary Laboratories Agency & School of Biological Science Royal Holloway, University of London “Remember to look up at the stars and not down at your feet” - Prof. Stephen Hawking I dedicate this thesis to My parents, John and Nicola Mappley Throughout all my endeavours, you believe in me Your support, encouragement and generosity are endless In loving memory of my grandmother, Hilda Leah ‘May’ Bull Always with me in spirit, if not in body You continue to inspire me Declaration of authorship I Luke John Mappley hereby declare that this thesis and the work presented in it is entirely my own. Where I have consulted the work of others, this is always clearly stated. Signed: Date: 4 Abstract The anaerobic spirochaete Brachyspira pilosicoli causes enteric disease in avian, porcine and human hosts, amongst others. Avian intestinal spirochaetosis (AIS), the resulting disease from colonisation of the caeca and colon of poultry by Brachyspira leads to production losses, with an estimated annual cost of circa £18 million to the commercial layer industry in the United Kingdom. A lack of knowledge of the metabolic capabilities and little genomic information for Brachyspira has resulted in a limited understanding of the pathobiology of this genus. In addition, an emergence of antibiotic resistance in Brachyspira, together with bans on the prophylactic use of antimicrobials in animal feed, drive an urgent requirement for alternative treatment strategies for diseases such as AIS. In the first intra-species genome comparison within the genus Brachyspira, these studies report the whole genome sequence of an avian strain of B. pilosicoli, B2904, and the incomplete genome sequence of a human strain of B. pilosicoli, WesB. Comparisons are made between the de novo sequenced strains and those of B. pilosicoli 95/1000, a pig strain and other available Brachyspira genome sequences from public databases. Furthermore, this study reports the first application of the high-throughput Biolog phenotype screening tool to Brachyspira for detailed phenotypic analysis and confirmation of metabolic deductions made from the genotypic data. Probiotics have been reported as protecting against infection with common enteric pathogens in livestock and in this study investigations into which aspects of the biology of Brachyspira they antagonise were undertaken. Lactobacilli reduced the growth and motility of B. pilosicoli and its ability to adhere and invade epithelial cells in vitro. Following these encouraging results, an in vivo intervention study was performed using a B. pilosicoli challenge model in poultry to elucidate the potential for probiotic intervention against AIS. This study demonstrated that when administered in drinking water, L. reuteri LM1, isolated from a healthy chicken, reduced all aspects of the clinical presentation of AIS. 5 Acknowledgments The past four years of work that have contributed to this thesis would not have been possible without the support and contribution of many people. I have been very fortunate to have worked towards this thesis under excellent supervision. To Prof. Roberto La Ragione, I am extremely thankful for your continuous and unconditional scientific, financial and moral support and for giving me the flexibility to develop into an independent scientist. To Prof. Martin Woodward, I am grateful to have shared in your enormous appetite for research and I have a great deal of respect for your true feedback, though at times frustrating, it was always fruitful. My thanks extend to Prof. Peter Bramley. During my studies, I was the privileged recipient of three travel grants from the Society of General Microbiology, two of which funded my attendance to international conferences that facilitated my first meeting with Prof. David Hampson and the third permitted a research visit to his laboratories at Murdoch University, Perth. To Prof. David Hampson and your family, I owe an enormous debt of gratitude for the hospitality, kindness and generosity you showed during my visit and also for some of the most meaningful and invaluable supervision and guidance that I received. At Murdoch, I owe great thanks to the people at the Centre for Comparative Genomics and the School of Veterinary and Biomedical Science for making me most welcome and notably to Prof. Matthew Bellgard, Dr. Nyree Phillips and Dr. Tom La, for your assistance and for permitting the use of additional data that contributed to the genome comparisons. I must especially thank Dr. Michael Black, without the wealth of time and expertise you dedicated and your willingness to provide help whenever asked, the comparative genomic research would have failed to be so prosperous. I am delighted to acknowledge Dr. Alistair Darby for your help with genome sequencing and assembly and for accommodating me on my numerous visits to the University of Liverpool. I acknowledge Prof. Julian Parkhill and Dr. Keith Turner for providing genome sequence data and Dr. Barry Bochner, for your generosity in providing additional Biolog resources and also for lending your knowledge and advice. My thanks extend to Dr. Alejandro Núñez and Bill Cooley for the help you both have 6 Acknowledgments given with histopathological and electron microscopical analysis and interpretation. I thank Andrew Steventon and David Welchman for your help and teaching me the basics of the isolation and culture of Brachyspira. I greatly acknowledge the receipt of funding from the British Egg Marketing Board Research and Education Trust and particularly Alan and Anne Beckett, for your moral and financial support. A special thank you to all my colleagues in the Department of Bacteriology at the Animal Health and Veterinary Laboratories Agency. It has been a wonderfully fulfilling and rewarding experience to work and study in this group and with some of my closest friends. To Christine Boinett, from day one your assistance and support has been greatly appreciated and I have been lucky to have found a friend in you from so early on in my studies. To Monika Tchórzewska, your assistance with in vitro and in vivo studies was endless, when it comes to helping others, you are selfless and in you, is someone who I can always count on. To Dr. Laura Searle, your guidance and assistance were second to none and I could not have asked for a better first lab partner and friend. To Manal AbuOun, I am eternally grateful for all your help and supervision, it is hard to think of an aspect of this work where your contribution was not key and I could not have wished to have work with a better postdoctorate. My experience would not have been so much fun without all your help, laughter and jokes. My deepest and most sincere thanks to my parents, John and Nicola, my sisters, Claire and Joanna and my late grandmother, May. Your tireless support, encouragement and enthusiasm has always been appreciated. Without your love and guidance, I would not have become the person I am today. You inspire me. I am forever in your debt and will love you always. Finally, this thesis would not have been accomplished without the faith, love and companionship of my best friend, soul mate and partner, Whitney. Thank you for your patience, your support, for being my strength and for sharing this achievement with me. You encourage me to aim for the stars and I cannot wait for our future. 7 Contribution of others David Welchman organised sample collection from affected flocks and Andrew Steventon supported in isolation in the of Brachyspira strains at the Animal Health and Veterinary Laboratories Agency, Winchester. Dr. Alistair Darby performed the genome sequencing for Brachyspira pilosicoli B2904 and provided assistance during its assembly and annotation. Prof. Julian Parkhill and Dr. Keith Turner provided the genome sequence for Brachyspira pilosicoli WesB. Prof. David Hampson, Dr. Nyree Phillips and Dr. Tom La provided the draft genome scaffolds for B. aalborgi 513T, B. alvinipulli C1T and B. intermedia HB60. Dr. Michael Black provided guidance and technical assistance to the comparative genomic analyses. The Cell and Tissue Culture Section at the Animal Health and Veterinary Laboratories Agency prepared HT29-16E monolayers for in vitro studies. The Animal Service Unit at the Animal Health and Veterinary Laboratories Agency assisted in day to day husbandry and veterinary input for the in vivo studies. Dr. Alejandro Núñez at the Animal Health and Veterinary Laboratories Agency assisted with post-mortem examinations and histopathological examination of stained tissues. Bill Cooley at the Animal Health and Veterinary Laboratories Agency processed cells and tissues from in vitro studies and undertook the electron microscopical examinations. 8 Table of contents Title page 1 Declaration 4 Abstract 5 Acknowledgements 6 Contribution of others 8 Table of contents 9 List of figures 17 List of tables 20 List of abbreviations 22 List of publications 24 Chapter 1. Introduction 25 1.1 Avian intestinal spirochaetosis 25 1.1.1 Definition of avian intestinal spirochaetosis 25 1.1.2 History of avian intestinal spirochaetosis 26 1.1.3 Significance of avian intestinal spirochaetosis 27 1.1.3.1 Economic 27 1.1.3.2 Public Health 27 1.1.4 Aetiology of avian intestinal spirochaetosis 27 1.1.5 Epidemiology of avian
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