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Downloaded from Using the Burrows Wheeler Aligner (BWA) Algorithm V0.7.13 (Andrews, 2010; Li and Durbin, 2009) The functional diversity and evolution of nuclear processes by Nicholas A. T. Irwin BSc. Hons, University of British Columbia, 2017 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in The Faculty of Graduate and Postdoctoral Studies (Botany) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) September 2020 © Nicholas A. T. Irwin, 2020 The following individuals certify that they have read, and recommend to the Faculty of Graduate and Postdoctoral Studies for acceptance, the dissertation entitled: The functional diversity and evolution of nuclear processes submitted by Nicholas A. T. Irwin in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Botany Examining Committee: Dr. Patrick J. Keeling, Professor, Department of Botany, UBC Supervisor Dr. LeAnn J. Howe, Professor, Department of Biochemistry and Molecular Biology, UBC Supervisory Committee Member Dr. Brian S. Leander, Professor, Department of Zoology and Botany, UBC Supervisory Committee Member Dr. Ivan Sadowski, Professor, Department of Biochemistry and Molecular Biology, UBC University Examiner Dr. James D. Berger, Professor Emeritus, Department of Zoology, UBC University Examiner Dr. Joel B. Dacks, Professor, Department of Medicine, University of Alberta External Examiner ii Abstract The nucleus is a defining characteristic of eukaryotic cells which not only houses the genome but a myriad of processes that function synergistically to regulate cellular activity. Nuclear proteins are key in facilitating core eukaryotic processes such as genome compaction, nucleocytoplasmic exchange, and DNA replication, but the interconnectedness of these processes makes them challenging to dissect mechanistically. Moreover, the antiquity of the nucleus complicates evolutionary analyses, limiting our view of nuclear evolution. Despite this, a comprehensive understanding of the function and evolution of nuclear processes is essential given their central importance in disease, basic cell biology, and eukaryotic evolution. In this dissertation, I argue that insights into nuclear biology and evolution can be obtained by examining eukaryotic diversity rather than relying solely on traditional model organisms. I begin by presenting an introduction to nuclear evolution and diversity, highlighting the existence of nuclear variation across eukaryotes from a systems perspective and underscoring the potential utility of biodiversity in studying nuclear processes (Chapter 1). In the following chapters, I test my hypothesis by examining the function and evolution of different processes in a subset of divergent nuclear systems: namely, chromatin in the dinoflagellate dinokaryon, nuclear pore complexes (NPCs) in the nucleomorphs of chlorarachniophytes and cryptophytes, and DNA replication in the ciliate macronucleus. In Chapter 2, I use an experimental evolutionary approach to investigate the drivers of histone depletion in dinoflagellates, revealing the capacity for viruses to shape cellular evolution and raising questions regarding the subfunctionalization of remnant dinoflagellate histones. In Chapter 3, I reconstruct the NPCs of endosymbiotically acquired nuclei, termed nucleomorphs, in silico, and predict a highly reduced pore structure, suggesting that a complex NPC may not be required for baseline nuclear function. Lastly, in Chapter 4, I examine the diversity of motile DNA replication systems in ciliates, highlighting new models for studying DNA replication and the capacity of cytoskeletal elements to coordinate nuclear organization and processes. Ultimately this work confirms the efficacy of examining diverse nuclear systems, provides insights into the biology and evolution of nuclear processes, and encourages a re-evaluation of how we view and select model organisms. iii Lay Summary Eukaryotic organisms, such as animals, plants, and fungi, are defined by the presence of a nucleus. Within all eukaryotic cells, the nucleus houses DNA which constitutes the genetic information defining all aspects of cellular life. Besides DNA, the nucleus contains a plethora of processes that manipulate how a cell's DNA is interpreted. These interpretations are fundamental to eukaryotic biology as they dictate how organisms respond to their environments, grow, and develop. Exploring nuclear biology is not only key to illuminating cellular function and evolution but is fundamental in understanding disease mechanisms. Research investigating the nucleus mostly relies on yeast and animal experimental models but the complexity of the nucleus warrants investigations into other organisms as they can provide unique perspectives into nuclear function. Here, I examine nuclear systems in diverse eukaryotic organisms, demonstrating how they can provide insights into nuclear function and the evolution and diversity of life. iv Preface Most of the work presented in this thesis has been published or submitted to peer-reviewed journals and was conducted in collaboration with other scientists. Here I outline the contributions and publications that correspond to each of the proceeding chapters. Chapter 1: Introduction The introduction constitutes an extended version of a manuscript intended to be a review article. I conducted literature reviews, designed the figures, and wrote the manuscript with input from Patrick Keeling. This chapter will be modified and revised to include recent discoveries stemming from this thesis and submitted as: Irwin, N. A. T. and Keeling, P. J. Nuclear biology: Mechanistic insights from eukaryotic diversity. In preparation. Chapter 2: Viral proteins as a potential driver of histone depletion in dinoflagellates This study was originally conceived and designed as an extension of a pilot project carried out in LeAnn Howe's lab during my bachelor's degree. I conducted all of the experiments and analyses with the exception of the Rpb3 chromatin immunoprecipitation (ChIP) and quantitative ChIP- polymerase chain reaction (PCR) experiments which were performed by Benjamin Martin, and the micrococcal nuclease digestions which were completed with the help of LeAnn Howe. Generation of expression constructs, the immunofluorescence experiment, and acquisition of synthetic genetic array (SGA) data were completed during my bachelor's degree (approximately 20% of the data). I wrote the manuscript and created all the figures and datasets with input from all of the authors. A version of this chapter has been published as: Irwin, N. A. T., Martin, B. J. E., Young, B. P., Browne, M. J. G., Flaus, A., Loewen, C. J. R., Keeling, P. J., and Howe, L. J. (2018). Viral proteins as a potential driver of histone depletion in dinoflagellates. Nat. Commun. 9, 1535. v Chapter 3: Extensive reduction of the nuclear pore complex in nucleomorphs This project was conceived and designed by Patrick Keeling and I. I developed the bioinformatic pipelines, conducted the analyses, designed the figures, and wrote the manuscript with input from Patrick Keeling. A version of this chapter has been published as: Irwin, N. A. T. and Keeling, P. J. (2019). Extensive reduction of the nuclear pore complex in nucleomorphs. Genome Biol. Evol. 11, 678–687. Chapter 4: Function and evolution of motile DNA replication systems in ciliates Chapter four was originally initiated as a phylogenetics project by Denis Lynn and William Bourland. After Denis Lynn's passing, I reoriented the project and altered its scope to be about the function and evolution of motile DNA replication systems. Denis Lynn isolated Licnophora macfarlandi and generated sequencing libraries from L. macfarlandi and Phacodinium metchnikoffi. William Bourland isolated and made microscopic observations of P. metchnikoffi including the scanning electron microscopy, histology, and 5-ethynyl-2′-deoxyuridine labeling experiments. I conducted all other analyses and experiments, wrote the manuscript, and made the figures (excluding Figure 13, 15, 16, and C1 which were made by William Bourland), with input from all authors. The manuscript has been published as: Irwin, N. A. T., Pittis, A. A., Mathur, V., Howe, L. J., Keeling, P. J., Lynn, D. H., and Bourland, W. A. (2020) The function and evolution of motile DNA replication systems in ciliates. Current Biology. In press. vi Table of Contents Abstract .......................................................................................................................................... iii Lay Summary ................................................................................................................................. iv Preface............................................................................................................................................. v Table of Contents .......................................................................................................................... vii List of Tables .................................................................................................................................. x List of Figures ................................................................................................................................ xi List of Symbols & Abbreviations ................................................................................................ xiii Acknowledgements .................................................................................................................... xviii Dedication ....................................................................................................................................
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