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Devon Radford Understanding the Encapsulins: Prediction and Characterization of Phage Capsid-like Nanocompartments in Prokaryotes by Devon Radford A thesis submitted in conformity with the requirements for the degree of Doctorate of Philosophy in Molecular Genetics Department of Molecular Genetics Faculty of Medicine University of Toronto © Copyright by Devon Radford 2015 Understanding the Encapsulins: Prediction and Characterization of Phage Capsid-like Nanocompartments in Prokaryotes Devon Radford Doctorate of Philosophy in Molecular Genetics Department of Molecular Genetics Faculty of Medicine University of Toronto 2015 Abstract Encapsulins are a distinct family of prokaryotic compartments, comprised of an icosahedral shell encapsulating a variety of enzymes. The encapsulin shell protein is similar in sequence and structure to the capsid protein of dsDNA tailed bacteriophages. Although found across diverse phyla of Bacteria and Archaea, few encapsulins were previously characterized. My thesis work utilized a bioinformatic approach to identify and investigate the functions of all encapsulins found in bacteria and Archaea. I found 590 encapsulins showing definite sequence similarity to the previously described encapsulins, which I refer to as “classical encapsulins”. I identified four new enzyme families strongly predicted to be classical encapsulin cargo enzymes: ferredoxins, rubrerythrin-like, Dps-bacterioferritin-like, and hemerythrin-like proteins. While most species encode encapsulin cargo proteins adjacent to the encapsulin gene, I discovered 113 species encoding cargo proteins in genomic regions far removed from the encapsulin gene. I also found 118 genomes encoding two or three different enzymes strongly predicted to be targeted to the same encapsulin. Genes encoding three protein families, radical ii SAM oxidoreductases, CutA1-like proteins and metalloproteases, are highly enriched near encapsulin genes, but without targeting motifs for direct encapsulation. In addition to classical encapsulins, I discovered 1060 novel putative encapsulins related to diverse families of phage capsids. The largest family of these novel encapsulins, with 986 proteins is larger than the classical encapsulin family, and conserves a sulphur metabolism operon encoding cysteine desulfurases, acetyltransferases, and rhodaneses. These activities are predicted to relieve sulphur restriction, and toxicity of cyanide and other oxidants. Overall, novel and classical encapsulins and their encapsulated enzymes are predicted to contribute to polyvalent cation dependent catalytic activities, and relieve heavy metal and cyanide toxicity. Phylogenies predicted capsids and encapsulins share intermingled ancestry. My work shows that encapsulins perform more diverse functions and are much more widely distributed than any other prokaryotic compartment. iii Acknowledgments I would like to thank the Canadian Institute of Health Research, the Natural Science and Engineering Research Council Alexander Graham Bell Doctoral Canada Graduate Scholarship program, and the Ontario Graduate Scholarship program for providing funding for this project. High performance computing resources supplied by Sharcnet and SciNet academic computing clusters. Many thanks are also due the technical and administrative staff of the University of Toronto, Department of Molecular Genetics. Special thanks to Diane Bona, Bianca Garcia, and Yurima Hidalgo specifically for their help and assistance throughout this project. I would also like to thanks all members of the Davidson and Maxwell labs, past and present for their input and constructive suggestions. Special thanks to Dr. Lia Cardarelli, Sarah Chan, Vuk Pavlovic, Dr. Lisa Pell, and Dr. Zhou Yu for the contributions to the phage and prophage database. Also thanks are due to Kris Hon and Kelly Reimer for assistance in optimizing bench work experimental designs. I would also like to thank the members of my supervisory committee who showed continued interest, critical insight and assistance throughout the project. In addition to my immediate supervisor, Dr. Alan Davidson, I would also like to acknowledge the insights and guidance provided by Dr. Karen Maxwell during the course of this project. Special mention is made to Linda Trouten-Radford and Don Radford for their tireless moral support, without which this project would have been impossible. I would also like to acknowledge the editorial assistance of Alan Davidson, my committee, and Linda Trouten-Radford in the revision and improvement of this thesis. iv Table of Contents Acknowledgments ............................................................................................................. iv List of Tables .................................................................................................................... vii List of Figures .................................................................................................................. viii List of Appendices ............................................................................................................. xi List of Defintions ............................................................................................................. xiii Chapter 1: Introduction and Background ...................................................................... 1 1.I Review of characterized prokaryotic compartments .................................................. 2 1.II Review of known properties of published encapsulins ............................................. 9 1.III Properties, similarities and differences of encapsulin and capsid-like structures .. 16 1.IV Bacteriophages profoundly influence prokaryotic evolution and physiology ....... 24 1.V Objectives ................................................................................................................ 26 Chapter 2: Identification of comprehensive population of encapsulins related to published examples............................................................................................................................ 29 2. Chapter Abstract: ...................................................................................................... 29 2. Introduction: ............................................................................................................. 30 2. Methods: .................................................................................................................... 31 2. Results: ...................................................................................................................... 37 2. Discussion: ................................................................................................................ 81 Chapter 3. Characterization of classical encapsulin-like families............................... 84 3. Chapter Abstract: ...................................................................................................... 84 3. Introduction: ............................................................................................................. 85 3. Methods: .................................................................................................................... 87 3. Results: ...................................................................................................................... 92 3. Discussion: .............................................................................................................. 142 Chapter 4: Families of distinct novel prokaryotic capsid-like compartments ......... 144 4. Chapter Abstract: .................................................................................................... 144 4. Introduction: ........................................................................................................... 145 4. Methods: .................................................................................................................. 147 v 4. Results: .................................................................................................................... 152 4. Discussion: .............................................................................................................. 175 Chapter 5: Conserved mechanisms of protein interaction produce the structural and functional similarities and differences existing between phage capsids and prokaryotic encapsulins ..................................................................................................................... 177 5. Chapter Abstract: .................................................................................................... 177 5. Introduction: ........................................................................................................... 178 5. Methods: .................................................................................................................. 183 5. Results: .................................................................................................................... 186 5. Discussion: .............................................................................................................. 203 Chapter 6: Caudovirales phage capsids share intermingled ancestry and descent with prokaryotic encapsulins ................................................................................................ 204 6. Chapter Abstract: .................................................................................................... 204 6. Introduction: ..........................................................................................................
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