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Insights Into the Role of the Flagellar Glycosylation System in Campylobacter Jejuni Phage-Host Interactions by Jessica Christia

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Insights Into the Role of the Flagellar Glycosylation System in Campylobacter Jejuni Phage-Host Interactions by Jessica Christia Insights into the role of the flagellar glycosylation system in Campylobacter jejuni phage-host interactions by Jessica Christiane Sacher A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Microbiology and Biotechnology Department of Biological Sciences University of Alberta © Jessica Christiane Sacher, 2018 Abstract Bacteriophages (phages) are the viruses that infect bacteria. Studying how phages interact with their hosts can inspire new ways of controlling bacterial pathogens and can highlight important facets of the biology of both organisms. Furthermore, phage-host characterization can inform exploitation of phages for therapeutics, diagnostics and research tools. Campylobacter jejuni is a deadly foodborne pathogen of humans, and its extensive surface structure glycosylation plays an important role in its virulence. In particular, C. jejuni flagella are required for colonization of its niche in the gastrointestinal tract of birds, and are also required for virulence in humans. C. jejuni devotes a substantial proportion of its genetic repertoire to flagellar biogenesis, which requires glycosylation with sialic acid-like sugars for assembly. Campylobacter phages tend to target either capsular polysaccharides or flagella, but little more than this is known about the factors governing Campylobacter phage-host interactions. My thesis describes the study of C. jejuni interactions with phages in the context of flagellar glycobiology. I found that C. jejuni phage NCTC 12673 interacts with host flagella and flagellar glycans in ways not previously described for other phage-host systems. Furthermore, this phage encodes a protein of unknown function (Gp047) with specific binding affinity for host flagellar glycans. I sought to determine how the C. jejuni flagellar glycosylation system and the NCTC 12673 phage each impact the biology of the other. I found that Gp047 inhibits growth of C. jejuni expressing flagellar acetamidino-modified pseudaminic acid glycans, that probing with Gp047 reveals previously unexplored diversity in ii C. jejuni flagellar glycans, and that Gp047 binding to motile, glycosylated flagella induces downregulation of pathways for cellular energy metabolism. I also found that C. jejuni pseudaminic acid biosynthesis (flagellar glycosylation) genes are required for bacteriophage NCTC 12673 infection, that a requirement for motility likely explains this dependence, and that oxidative stress sensitivity may explain the reduced ability of phage NCTC 12673 to plaque on non-motile C. jejuni mutants. Finally, I found that expression of the flagellar glycan binding protein Gp047 correlates with a lack of plaquing by phage NCTC 12673 on non- motile C. jejuni cells, providing an interesting foundation for future research. Overall, my work points toward flagellar glycosylation as an important factor affecting C. jejuni phage-host dynamics, and provides insight into the role of a flagellar glycan-binding phage protein in these interactions. These findings contribute to the fields of phage biology and bacterial glycobiology by providing insight into how a Campylobacter phage interacts with its heavily glycosylated host. iii Preface Chapter 2 was published as Sacher, J. C.; Flint, A.; Butcher, J.; Blasdel, B.; Reynolds, H. M.; Lavigne, R.; Stintzi, A.; Szymanski, C. M. Transcriptomic analysis of the Campylobacter jejuni response to T4-like phage NCTC 12673 infection. Viruses 2018, 10, 332. I designed and performed the experiments, analyzed the data, and wrote the paper. Annika Flint and Hayley Reynolds performed experiments, James Butcher, Bob Blasdel and Rob Lavigne provided guidance, analyzed the data and edited the manuscript, Alain Stintzi contributed materials, guided the experiments, and analyzed the data, and Christine Szymanski supervised and funded the project, analyzed the data and edited the manuscript. Chapter 3 was published as Javed, M. A.; Sacher, J. C.; van Alphen, L. B.; Patry, R. T.; Szymanski, C. M. A flagellar glycan-specific protein encoded by Campylobacter phages inhibits host cell growth. Viruses 2015, 7, 6661-6674. I contributed the data for 4/6 figures, contributed 1/3 tables, helped analyze the data, edited the manuscript, and wrote part of the discussion. Afzal Javed designed and performed experiments, provided training, analyzed the data and wrote the original version of the manuscript. Lieke van Alphen and Robert Patry performed experiments. Christine Szymanski supervised and funded the project, analyzed the data and edited the manuscript. A version of Chapter 4 will be submitted for publication as Sacher, J. C.; Shajahan, A.; Patry, R. T.; Butcher, J.; Flint, A.; Stintzi, A.; Azadi, P.; Szymanski, C. M. Novel insights into Campylobacter jejuni flagellar glycan diversity revealed by probing with a conserved glycan- specific bacteriophage binding protein. I designed the experiments, analyzed the data and wrote the chapter. Asif Shajahan performed the MS experiments and analyzed the data. Rob iv Patry and Annika Flint performed experiments, James Butcher provided guidance and analyzed the data, Alain Stintzi and Parastoo Azadi contributed materials, guided the experiments, and analyzed the data, and Christine Szymanski supervised and funded the project, analyzed the data and edited the manuscript. A version of Chapter 5 will be submitted for publication as Sacher, J. C.; Javed, M. A.; Reynolds, H. M.; Butcher, J.; Flint, A.; Stintzi, A.; Szymanski, C. M. Campylobacter jejuni phage NCTC 12673 dependence on flagellar glycosylation and flagellar motor genes is overcome by a single escape mutant. I designed the experiments, analyzed the data and wrote the manuscript. Hayley Reynolds and Annika Flint performed experiments, James Butcher provided guidance and analyzed the data, Alain Stintzi contributed materials, guided the experiments, and analyzed the data, and Christine Szymanski supervised and funded the project, analyzed the data and edited the manuscript. A version of Appendix I was published as Sacher, J. C.; Yee, E.; Szymanski, C. M.; Miller, W. G. Complete genome sequences of three Campylobacter jejuni phage-propagating strains. Genome Announc. 2018, 6, e00514-18. A version of Appendix II of this thesis was published as Sacher, J. C., Yee, E., Szymanski, C. M., & Miller, W. G. Complete genome sequence of Campylobacter jejuni strain 12567, a livestock-associated clade representative. Genome Announc. 2018, 6, e00513-18. I grew the strains, extracted and submitted gDNA for Illumina sequencing, assembled strain information, initiated the submission of the genomes to NCBI, and wrote the first draft of the Genome Announcement. Emma Yee prepared gDNA for PacBio sequencing. William Miller annotated the genomes, contributed reagents, analyzed the data, and aided in preparing the genomes for submission and the Genome Announcement for v publication. Christine Szymanski supported and guided the projects, analyzed the data and edited the Genome Announcements. vi Acknowledgements I would like to thank my supervisor, Christine Szymanski, for her incredible mentorship over the last 9 years. From my first day meeting you back in 2009, when I was a 3rd year undergraduate student eager to take your Microbial Glycobiology class, I was inspired by your enthusiasm and passion for science. Since then, your excitement for science has never seemed to waver, no matter how close we got to deadlines or how far into the wee hours of the morning it was. I have learned more than I can describe from your mentorship – about working with people, speaking in public, prioritizing, finding motivation, thinking through complex sets of data, and coming up with exciting new plans no matter what the experimental outcome. I don’t think there’s a person on Earth who could find the silver lining in a situation faster or more consistently than you. I am so thankful for all you have done to help me become the scientist I am today. I would also like to thank my committee members, Lisa Stein and Stefan Pukatzki, for their kindness, enthusiasm, support and guidance. I always looked forward to meeting with you about my projects, and always came out of those meetings with a list full of excellent experimental suggestions and the feeling that the possibilities for my project were endless. I am so grateful for the colleagues I was lucky enough to go through this experience with, both at the University of Alberta and during my time spent at the Universities of Ottawa and Georgia. I am particularly thankful for the mentorship, unwavering patience and friendship of David Simpson, Afzal Javed, Denis Arutyunov, Harald Nothaft, Ritika Dwivedi, Cory Wenzel and Bernadette Beadle. I will always take joy in talking science or life with any one of you, and have countless memories that I will treasure. Jolene, Rob, Justin, Cody and Clay, you have been incredible people to have by my side in the lab, and it will take me a very long time to get used to life without you each day. Thank you all for putting up with my tendencies to hoard lab supplies, and for being willing to laugh about it each time. I adore vii you all, and I’ll treasure your friendship for life. Thank you also to the undergraduate students I was fortunate enough to mentor: Lily Li, Stephanie Guerra, and Hayley Reynolds. Your enthusiasm in the lab made coming to work such a joy! Somehow each of you were able to convert my sporadic and sometimes conflicting instructions into amazing progress in the lab, and your help with moving our projects
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