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Exploring the Phylodynamics, Genetic Reassortment and RNA Secondary Structure Formation Patterns of Orthomyxoviruses by Comparative Sequence Analysis

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Exploring the Phylodynamics, Genetic Reassortment and RNA Secondary Structure Formation Patterns of Orthomyxoviruses by Comparative Sequence Analysis Exploring the Phylodynamics, Genetic Reassortment and RNA Secondary Structure formation patterns of Orthomyxoviruses by Comparative Sequence Analysis By Fredrick Nzabanyi Nindo (BSc, MSc) Supervisor Assoc Prof Darren Martin Thesis presented for the degree of DOCTOR OF PHILOSOPHY In theUniversity Department of Integrative of Cape Biomedical Town Sciences Faculty of Health Sciences, UNIVERSITY OF CAPE TOWN November 2019 The copyright of this thesis vests in the author. No quotation from it or information derived from it is to be published without full acknowledgement of the source. The thesis is to be used for private study or non- commercial research purposes only. Published by the University of Cape Town (UCT) in terms of the non-exclusive license granted to UCT by the author. University of Cape Town ACKNOWLEDGEMENTS My first acknowledgements goes to my supervisor Associate Professor Darren Patrick Martin for giving me an opportunity to pursue PhD under guidance and encouragement throughout the research period without which this work would not have come to completion. I particularly wish to thank him for giving me the freedom to explore research agenda of my choice but with his mentorship. I wish also to acknowledge the Darren Lab’s members especially Dr Brejnev Muhire for his help with debugging of some scripts when the going got tough and not forgetting Dr Gordon Harkins of SANBI, UWC, for his useful discussions on the emerging approaches and techniques in phylodynamics in the era of sequence data deluge. My sincere thanks also goes to the members of CBIO group who are many to name individually here as computational biology research family, they played a role in the realization of this work. Further, acknowldgements also goes to Ayton and Gerrit (the senior systemsdeveloper and Bioinformatics engineer) who came to my rescue by offering me computation space on the CBIO cluster when I needed it most to bring to completion my analyses. I thank God for the wonderful parents and members of my extended family in Kenya who have always believed in me, for their encouragement to always aim high. I also thank God for wonderful friends and the Cape Town community that I have had wonderful interactions and who played a role to make my stay hospitable during the course of my studies. May you remain blessed. Last but not least, I wish to thank the Carnegie Corporation of New York for their generous funding support for the prestigious PhD scholarship for research in Infectious Diseases under the Next Generation of Academics in Africa (NGAA) programme for tenable at the Institute of Infectious Diseases and Molecular Medicine, Faculty of Health Sciences, University of Cape Town and the Polimyelitis Research Foundation (PRF) of South Africa for their PhD Bursary for research in Medical Virology in South Africa. ii DEDICATION I dedicate this dissertation to my lovely wife, Eva and courageous sons; Keith and Danny in for their love, resilience and and unlimited support during my entire study period. iii DECLARATION I, Fredrick Nzabanyi Nindo, hereby declare that the work on which this thesis is based is my original work (except where acknowledgements indicate otherwise) and that neither the whole work nor any part of it has been, is being,or is to be submitted for another degree in this or any other university. I authorize the University to reproduce for the purpose of research either whole or any portion of the contents in any manner whatsoever. Signature:… Date: 12.02.2020 iv ABSTRACT RNA viruses are among the most virulent microorganisms that threaten the health of humans and livestock. Among the most socio-economically important of the known RNA viruses are those found in the family Orthomyxovirus. In this era of rapid low cost genome sequencing and advancements in computational biology techniques, many previously difficult research questions relating to the molecular epidemiology and evolutionary dynamics of these viruses can now be answered with ease. Using sequence data together with associated meta-data, in chapter two of this dissertation I tested the hypothesis that the Influenza A/H1N1 2009 pandemic virus was introduced multiple times into Africa, and subsequently dispersed heterogeneously across the continent. I further tested to what degree factors such as road distances and air travel distances impacted the observed pattern of spread of this virus in Africa using a generalised linear model based approach. In chapter three, I set out to test two hypotheses: (1) that there is no difference in the frequency of reassortments among the segments that constitute influenza virus genomes; and (2) that there is epochal temporal reassortment among influenza viruses and that all geographical regions are equally likely sources of epidemiologically important influenza virus reassortant lineages In chapter four of this thesis, I explored the formation of RNA secondary structures within the genomes of orthomyxoviruses belonging to five genera: Influenza A, B and C, Infectious Salmon Anaemia Virus and Thogotovirus using in silico RNA folding predictions and additional molecular evolution and phylogenetic tests to show that structured regions may be biologically functional. The presence of some conserved structures across the five genera is likely a reflection of the biological importance of these structures, warranting further investigation regarding their role in the evolution and possible development of antiviral resistance. The studies herein demonstrate that pathogen genomics-based analytical approaches are useful both for understanding the mechanisms that drive the evolution and spread of rapidly evolving viral pathogens such as orthomyxoviruses, and for illuminating how these approaches could be leveraged to improve the management of these pathogens. v CONTENTS Acknowledgements .................................................................................................................. ii Dedication ............................................................................................................................... iii Declaration............................................................................................................................... iv Abstract ..................................................................................................................................... v List of Figures ........................................................................................................................... x List of Tables .......................................................................................................................... xii List of Appendices ................................................................................................................. xiv List of Acronyms .................................................................................................................... xv Chapter 1 .................................................................................................................................. 1 Introduction and Literature Review ...................................................................................... 1 1.1 Introduction .............................................................................................................................. 1 1.1.1 Overall aims and Objectives ...................................................................................................... 2 1.1.2 Thesis Structure ............................................................................................................................. 3 1.2 Literature Review .................................................................................................................... 4 1.2.0 Overview of orthomyxovirus taxonomy ................................................................................ 4 1.2.1 Influenza A viruses ....................................................................................................................... 6 1.2.2 Influenza B viruses ....................................................................................................................... 7 1.2.3 Influenza C viruses ....................................................................................................................... 8 1.2.4 Infectious Salmon Anemia Virus (Isavirus) ...................................................................... 10 1.2.5 Thogoto Virus (THOV) ........................................................................................................... 11 1.2.6 Quaranjaviruses .......................................................................................................................... 11 1.3 Genomic organisation.......................................................................................................... 12 1.3.1 Membrane protein encoding segments ................................................................................ 13 1.3.2 Internal segments ....................................................................................................................... 13 1.4. Evolutionary mechanisms that impact the genetic diversity of Orthomyxoviruses13 1.4.1 Point mutations ........................................................................................................................... 14 1.4.2 Reassortment and recombination .......................................................................................... 14 1.4.3 RNA folding patterns in
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