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Recombinase in Trio (RIT) Elements in Bacterial Genomes: Assessing the Distribution and Mobility of a Novel Yet Widespread Set of Mobile Genes

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Recombinase in Trio (RIT) Elements in Bacterial Genomes: Assessing the Distribution and Mobility of a Novel Yet Widespread Set of Mobile Genes Recombinase in Trio (RIT) Elements in Bacterial Genomes: Assessing the Distribution and Mobility of a Novel yet Widespread Set of Mobile Genes. by Nicole Dorothy Ricker A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Physical and Environmental Sciences University of Toronto Scarborough © Copyright by Nicole Ricker 2016 Recombinase in Trio (RIT) Elements in Bacterial Genomes: Assessing the Distribution and Mobility of a Novel yet Widespread Set of Mobile Genes. Nicole Dorothy Ricker Doctor of Philosophy Department of Physical and Environmental Sciences University of Toronto Scarborough 2016 Abstract The research performed over the course of my doctorate training outlines the environmental distribution, mobility, expression and potential role of a newly described family of mobile elements as well as providing valuable information on the challenges and potential benefits of environmental metagenomics. Sequencing technologies have evolved considerably over the course of this work, and evaluating the limitations and opportunities provided by these evolving technologies has formed a significant portion of my thesis work. The remainder of the work has been dedicated to understanding the distribution and mechanisms of Recombinase in Trio (RIT) elements, a previously underappreciated mobile element found in a large diversity of strains, but predominantly in non- pathogenic bacteria. Recombinase in Trio (RIT) elements contain three tyrosine-based site-specific recombinases and display a characteristic gene order and repeat architecture that is conserved across 7 bacterial phyla (Van Houdt et al. 2006; Van Houdt et al. 2012; Ricker et al. 2013). RIT elements have been postulated to be mobile due to the occurrence of multiple identical copies within individual genomes, and are commonly found on plasmids and in genomic islands, including plant symbiosis and catabolic islands. The ability of RITS to excise and relocate themselves was tested using a variety of mating experiments. Although the determination of a potential target site sequence was initially elusive, the discovery that the RIT element also included a 20 bp palindrome adjacent to one of the terminal inverted repeats allowed for the alignment of the target genes and revealed the original target site sequence. Subsequently, RIT element mobility was observed during conjugation and the transformants analyzed provided some insight into the mechanism of recombination. Finally, environmental sampling was performed on Southern Ontario streams in order to develop a methodology for evaluating the mobilome community of bacterial communities. ii Acknowledgments No great achievement is accomplished without having a thousand people to thank. It would be impossible to list all the people that have helped, supported and encouraged me over the years and I hope that you truly understand my gratitude for each and every one of you. I want to especially thank my outstanding supervisor, Roberta Fulthorpe, for all of your amazing mentorship over the past 6 years. You have provided me with encouragement and support when I felt unsure, clarity and direction when I was muddled, and a firm kick when I was stalled. Not to mention physical labour and beautiful lake scenery for balance, and the insight to recognize an amazing opportunity when it came knocking. I could not ask for a better supervisor for my PhD, or a better mentor for my career. I would also like to thank my committee members (Don Jackson and William Navarre) for their outstanding insight and recommendations throughout the project, as well as their patience and encouragement. To my husband Toby – you have been my rock throughout my PhD and have done so much more than I ever could have asked of you. From sampler design, creation and installation to learning site specific recombination mechanisms and moving to Belgium (twice!), you’ve put in the blood, sweat and tears of this PhD and I am truly blessed to have such a wonderful partner in my life. Thanks also to my Mom for her endless support including hopping on a plane last minute to help with the first move to Belgium – and for helping to make sure I didn’t fall apart once we got there. Thanks to my Dad for assisting with all the reference site samplers and reminding me why I’m in this field by constantly making me defend science; and to my siblings for keeping me grounded while also reminding me that I could do this. My time at UTSC has been filled with amazing people and opportunities that I had never anticipated. I want to thank everyone at the Fulthorpe lab (past and present) for all your support and encouragement, and for putting up with endless talks about RIT elements. I especially have to thank Tony, Roxana and Rosemary for all your dedication and friendship. Last but not least, I am so grateful for having had the opportunity to work with Rob Van Houdt and Bernard Hallet, as well as Ann Provoost, Kristel Mijnendonckx and all the other members of the SCK•CEN and to the W. Garfield Weston Foundation for providing funding for this international collaboration. iii Table of Contents Acknowledgments .......................................................................................................................... iii Table of Contents ........................................................................................................................... iv List of Tables ............................................................................................................................... viii List of Figures ................................................................................................................................. x List of Appendices ....................................................................................................................... xiii Chapter 1 Introduction .................................................................................................................... 1 1.1 References ........................................................................................................................... 3 Chapter 2 The Role of Mobile Genetic Elements in Prokaryotic Adaptation ................................ 5 2 Horizontal Gene Transfer ........................................................................................................... 5 2.1 Intracellular MGEs .............................................................................................................. 7 2.2 Intercellular MGEs .............................................................................................................. 9 2.3 Impact on Genome Evolution ........................................................................................... 12 2.4 References ......................................................................................................................... 15 Chapter 3 The Limitations of Draft Assemblies for Understanding Prokaryotic Adaptation and Evolution ........................................................................................................................... 21 3 Introduction .............................................................................................................................. 21 3.1 Methods ............................................................................................................................. 24 3.2 Results ............................................................................................................................... 25 3.2.1 Assembly Quality for Cupriavidus metallidurans CH34 ..................................... 25 3.2.2 Contigs terminate at repeated elements and mobile elements .............................. 29 3.2.3 Fragmentation is greatest at genomic island sites ................................................. 30 3.2.4 Investigating the relative contribution of multiple replicons or presence of documented mobility genes by comparison with other strains ............................. 32 3.2.5 Fragmentation Evident in Real Data ..................................................................... 36 3.3 Discussion ......................................................................................................................... 38 iv 3.4 Acknowledgements ........................................................................................................... 42 3.5 References ......................................................................................................................... 43 Chapter 4 Phylogeny and Organization of Recombinase in Trio (RIT) Elements ....................... 47 4 Introduction .............................................................................................................................. 47 4.1 Methods ............................................................................................................................. 48 4.2 Results and Discussion ..................................................................................................... 48 4.2.1 Abundance and Occurrence in Database .............................................................. 48 4.2.2 RIT Structure and Organization ............................................................................ 51 4.2.3 Inferred RIT Functionality .................................................................................... 53 4.2.4 Evidence for RIT Mobility Within Closely Related Strains ................................
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