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Anti-Crisprs and CRISPR-Cas: Characterization and Biotechnology Anti-CRISPRs and CRISPR-Cas: Characterization and biotechnology by Marios Mejdani A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Biochemistry University of Toronto © Copyright by Marios Mejdani 2019 Anti-CRISPRs and CRISPR-Cas: Characterization and biotechnology Marios Mejdani Doctor of Philosophy Department of Biochemistry University of Toronto 2019 Abstract Bacteria and phages (bacterial specific viruses) have been undergoing an evolutionary arms race for billions of years, whereby bacteria evolve mechanisms to inhibit phage infection and phages evolve mechanisms to evade bacterial defenses. Consequently, there are several mechanisms used by bacteria to inhibit phage infection. These include inhibiting phage adsorption, restriction modification systems, and the more recently discovered CRISPR-Cas immune systems. Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR) loci together with their accompanying CRISPR-associated (Cas) genes form the only known bacterial adaptive defense mechanism that effectively protects against the transfer of mobile genetic elements (MGEs) such as bacteriophages. CRISPR-Cas systems use an RNA-guided nuclease to bind and cleave foreign DNA, presenting a powerful barrier to phage infection. This strong evolutionary barrier led phages to evolve small protein inhibitors of CRISPR-Cas called anti-CRISPRs. In the first section of my work, I characterize the structure, function, and mechanism of action for an anti-CRISPR that inhibits the type I-E CRISPR-Cas system of Pseudomonas aeruginosa strain 4386. I show that beyond simply inhibiting the CRISPR-Cas system, anti-CRISPR AcrIE2 converts the CRISPR-Cas system from a DNA degradation ii complex to a transcriptional regulator. This modification suggests that anti-CRISPR proteins may function to do more than simply inhibit CRISPR-Cas targeting. Although CRISPR-Cas systems are a manifestation of the evolutionary arms race between bacteria and phages, CRISPR-Cas systems have also been used for genome editing in various organisms for research purposes. Considering this previous work, I developed a type I-E and type II-A CRISPR-Cas genome editing system to manipulate the genome of different P. aeruginosa strains for research. In the second section of my work, I discuss the methods I developed to efficiently edit the genome of P. aeruginosa . My work on genome editing in P. aeruginosa has and will allow for the development of new P. aeruginosa mutants for research purposes. Collectively, my work provides insight into the evolutionary interactions between phages and bacteria in the context of CRISPR-Cas and anti-CRISPRs. Moreover, it provides a genome editing tool for future P. aeruginosa studies. iii Acknowledgments I would like to acknowledge my supervisor, Dr. Alan Davidson, for his excellent support and mentorship over the last five years. Alan has steered me in the right direction both within the lab and outside of it. I have certainly benefited from his advice over the years. I would also like to thank Dr. Karen Maxwell for her expertise in suggesting ideas and helping troubleshoot experiments. To my supervisory committee composed of Dr. William Navarre and Dr. Angus McQuibban. I want to thank you for your insightful ideas. Will, the ability to walk into your office and just throw ideas at you when Alan wasn’t around was truly invaluable. Angus, your relaxed personality and attention to detail has helped me reach my Ph. D. today. Now to thank the members of the lab. Thank you everyone for creating a wonderful atmosphere to work in. A special thanks to April Pawluk for training me at the start of my journey. I would also like to thank Joe Bondy-Denomy for his insight and scientific advice in my early years. Kristina deserves a special thanks in this acknowledgment, thank you for helping me fully develop the Cas9 genome editing tool and more so, thank you for being a friend I could always count on. Also, I would like to thank Kristina for helping me put overnights in the incubator when I needed it. To Vasu, Chidozie, Eric, and Brian, thank you for your help dealing with issues both within and outside of the lab, you are all true friends. Now for people and friends outside the lab, I want to thank people from Grant Brown’s lab for the help, care, and support they gave me relatively early in my M. Sc. / Ph. D. I would also like to generally acknowledge people in the Moraes lab, the Nodwell lab, the Cowen lab, and the Ensminger lab. iv Finally, and importantly my parents. I have watched them work so hard during their life all so that I could have opportunities not afforded to them. These are true heroes in today’s world and nothing short of it. They have taught me to work hard and work smart, be confident in myself and my abilities, and allow no one to stand in my way. Lessons that I consider to be the most invaluable in the world I see today. v Table of Contents Contents Acknowledgments ........................................................................................................................ iv Table of Contents ......................................................................................................................... vi List of Tables ................................................................................................................................ ix List of Figures .................................................................................................................................x List of Abbreviations .................................................................................................................. xii List of Appendices (if any) ........................................................................................................ xiii Chapter 1 ........................................................................................................................................1 1.1 Overview .............................................................................................................................1 1.2 Bacteria and Mobile Genetic Elements (MGEs) .............................................................2 1.3 Bacteriophages ...................................................................................................................4 1.4 Co-evolution of bacteria and phages ................................................................................7 1.5 CRISPR-Cas systems (Class I and Class II) ....................................................................8 1.5.1 Type I-E and Type II-A CRISPR-Cas mechanisms .........................................10 1.6 Discovery of CRISPR-Cas inhibitors .............................................................................13 1.6.1 Anti-CRISPR mechanisms ..................................................................................14 1.7 CRISPR-Cas: As a biotechnological tool .......................................................................17 1.8 CRISPR-Cas used for genome editing ...........................................................................17 1.8.1 Type I-E CRISPR-Cas mechanism for biotechnology .....................................20 1.8.2 Type II-A CRISPR-Cas mechanism for biotechnology ....................................21 1.9 Thesis Objectives ..............................................................................................................21 1.10 Thesis Outline ...................................................................................................................22 Chapter 2 .................................................................................................................................23 Anti-CRISPR AcrIE2: A novel mechanism of CRISPR-Cas inhibition .................................23 vi 2.1 Acknowledgements ..........................................................................................................23 2.2 Abstract .............................................................................................................................23 2.3 Anti-CRISPR AcrIE2 ......................................................................................................24 2.4 Results ...............................................................................................................................26 2.4.1 AcrIE2 functional residues..................................................................................26 2.4.2 AcrIE2 interacting partners................................................................................35 2.4.3 AcrIE2 mutants ....................................................................................................36 2.4.4 AcrIE2 inhibits DNA degradation but permits DNA binding .........................38 2.4.5 AcrIE2 is responsible for CRISPR-Cas dependent transcriptional repression and activation ....................................................................................44 2.5 Discussion..........................................................................................................................48 2.6 Materials and Methods ....................................................................................................52 2.6.1 Phage propagation and bacterial growth ..........................................................52 2.6.2 Phage spotting assays ...........................................................................................53 2.6.3 Lysogen formation ...............................................................................................53
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