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Circulation of Pathogenic Spirochetes in the Genus Borrelia

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Circulation of Pathogenic Spirochetes in the Genus Borrelia CIRCULATION OF PATHOGENIC SPIROCHETES IN THE GENUS BORRELIA WITHIN TICKS AND SEABIRDS IN BREEDING COLONIES OF NEWFOUNDLAND AND LABRADOR by © Hannah Jarvis Munro A Thesis submitted to the School of Graduate Studies in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biology Memorial University of Newfoundland May 2018 St. John’s, Newfoundland and Labrador ABSTRACT Birds are the reservoir hosts of Borrelia garinii, the primary causative agent of neurological Lyme disease. In 1991 it was also discovered in the seabird tick, Ixodes uriae, in a seabird colony in Sweden, and subsequently has been found in seabird ticks globally. In 2005, the bacterium was found in seabird colonies in Newfoundland and Labrador (NL); representing its first documentation in the western Atlantic and North America. In this thesis, aspects of enzootic B. garinii transmission cycles were studied at five seabird colonies in NL. First, seasonality of I. uriae ticks in seabird colonies observed from 2011 to 2015 was elucidated using qualitative model-based statistics. All instars were found throughout the June-August study period, although larvae had one peak in June, and adults had two peaks (in June and August). Tick numbers varied across sites, year, and with climate. Second, Borrelia transmission cycles were explored by polymerase chain reaction (PCR) to assess Borrelia spp. infection prevalence in the ticks and by serological methods to assess evidence of infection in seabirds. Of the ticks, 7.5% were PCR-positive for B. garinii, and 78.8% of seabirds were sero-positive, indicating that B. garinii transmission cycles are occurring in the colonies studied. Five I. uriae from two seabird colonies were positive for the Asian strain of the Lyme disease-causing species, B. bavariensis, which has previously only been described from the terrestrial realm associated with rodent reservoirs. The complete microbiome of ticks from two seabird colonies was also explored, which was consistent with PCR-based estimates of Borrelia spp. prevalence and identified infections with Coxiella and Ehrlichia spp., which may also be tick-borne. Third, the phylogenetic relationships of B. garinii found in ii the study samples, with B. garinii from elsewhere in the world, were explored using concatenated multi-locus sequence typing (MLST) gene sequences. This revealed close relationships between B. garinii in Eurasia and seabird colonies in NL. These results add to our knowledge of all levels of this complex, under-studied system, and help to inform us on how seabirds facilitate the global dispersion of B. garinii and other Borrelia species. iii ACKNOWLEDGEMENTS I would like to acknowledge the contributions of numerous individuals who provided assistance with sample collection, sample organization and data management. I would like to thank Alex Bond, Donald Pirie-Hay, Amy-Lee Kouwenberg, Paul Regular, Michelle Fitzsimmons, Natasha Walzthoni, Laura Tranquilla McFarland, Sheena Roul, Rafael Teixeira, Esther London, Robyn Butt, Holly Hogan and Ludmila Ferreira Gouveia. Pierre Ryan, Sabina Wilhelm (Canadian Wildlife Service), Dave Fifield, and Greg Robertson (Environment Canada) who were crucial for providing access to seabird colonies, aid in capture of birds, and assisting in sample collection. Further, I would like to thank the members of the Lang Lab, particularly Marta Canuti for her never ending support with PCR and other molecular techniques, as well as support in phylogenetic analysis. I would also like to thank Samir Mechai and Joost Verhoeven for support in analysis of MLST and microbiome data. I would like to thank Robbin Lindsay and Antonia Dibernardo from the National Microbiology Lab for support in setting up and designing screening protocols. They were always happy to answer any of my questions about PCR and confirming my results. Invaluable support was provided by Thierry Boulinier and Karen McCoy at Université Montpellier and their student, Amandine Gamble, by performing serological analysis of seabird blood samples. iv Finally, I would like to thank my supervisory committee: Andrew Lang, Hugh Whitney, Greg Robertson and Nick Ogden for all their encouragement, support and patience throughout this project. Support for this work was provided by the Government of Newfoundland and Labrador (Department of Natural Resources), Environment Canada, and the Public Health Agency of Canada (PHAC). Research in the Lang lab is supported by funding from Natural Sciences and Engineering Research Council (NSERC). I was supported by funding from PHAC and Government of Newfoundland and Labrador (Department of Natural Resources) and graduate student fellowships from the Memorial University of Newfoundland School of Graduate Studies. Fieldwork in Labrador was supported by a Northern Scientific Training Program grant (Government of Canada, Department of Indian and Northern Affairs). v TABLE OF CONTENTS Table of Contents ............................................................................................................... vi List of Tables ...................................................................................................................... x List of Figures .................................................................................................................... xi List of Abbreviations ........................................................................................................ xiii List of Appendices ............................................................................................................. xv Chapter 1: Introduction and Overview ............................................................................... 1 1.1. Introduction .......................................................................................................... 1 1.1.1. General introduction ..................................................................................... 1 1.1.1. Migratory species .......................................................................................... 2 1.1.2. The system for my thesis .............................................................................. 3 1.1.3. Location of study .......................................................................................... 8 1.2. Thesis overview.................................................................................................... 9 1.3. Co-authorship statement ..................................................................................... 11 Chapter 2: Seasonality of Ixodes uriae in seabird colonies of Newfoundland and Labrador .................................................................................................................................... 13 2.1. Abstract .............................................................................................................. 13 2.2. Introduction ........................................................................................................ 14 2.3. Methods .............................................................................................................. 16 2.3.1. Ethics........................................................................................................... 16 2.3.2. Tick collection ............................................................................................ 17 2.3.3. Statistical analysis ....................................................................................... 18 2.4. Results ................................................................................................................ 21 2.4.1. Larval counts ............................................................................................... 21 2.4.2. Nymphal counts .......................................................................................... 22 2.4.3. Adult counts ................................................................................................ 23 2.4.4. Proportion of adult females ......................................................................... 23 2.4.5. Proportion of engorged larvae .................................................................... 24 vi 2.4.6. Proportion of engorged nymphs.................................................................. 24 2.4.7. Proportion of engorged adult females ......................................................... 25 2.5. Discussion .......................................................................................................... 25 2.5.1. Variation between years .............................................................................. 26 2.5.2. Host density ................................................................................................ 27 2.5.3. Colony ......................................................................................................... 28 2.5.4. Seasonal patterns ......................................................................................... 29 Chapter 3: Ixodes uriae associated bacteria within seabird colonies of Newfoundland and Labrador ............................................................................................................................. 47 3.1. Abstract .............................................................................................................. 47 3.2. Introduction ........................................................................................................ 49 3.3. Methods .............................................................................................................
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