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Ling-Shan Yu Broad-scale phylogenomics reveals insights into retroviral origin and gammaretrovirus-host evolution Ling-Shan Yu A dissertation submitted for the degree of Doctor of Philosophy at Imperial College London December 2015 1 Abstract The Retroviridae is a family of single-stranded positive-sense animal viruses united by a unique mechanism of replication. Numerous studies have demonstrated the host diversity and host–retrovirus evolutionary history of the Retroviridae. However, in the past it has been difficult to gain a deeper understanding owing to the lack of sufficient host genomic data. Recent advances in whole-genome sequencing and bioinformatics technologies have enabled the collection of high-quality vertebrate genomic data. Broad-scale in silico screening of vertebrate genomes provides numerous opportunities to analyse retroviral origin and evaluate the risks and limitations of horizontal transmissions between different host species. In Chapters 2 and 3, I expand our current understanding of retroviral diversity in lower vertebrates and identify the host range boundary of the Retroviridae. I report the discovery of a basal retrovirus within the genome of the lamprey (Petromyzon marinus). No retroviruses were identified within other basal chordates, such as hagfishes, molluscs and sponges. This suggests that members of the Retroviridae are restricted to the lamprey and other phylogenetically higher vertebrates, and the host range boundary of this virus family has been potentially identified. In addition, this study identified extensive retroviral diversity in the basal vertebrates. The phylogenetic results show that at least three independent invasions have occurred in cartilaginous fish and the coelacanth. In Chapter 4, I investigate the gammaretroviral diversity and evolutionary history of mammalian genomes by combining the data of viral hosts and viral sequences. The study provides insights into the retrovirus–host evolution history. Six horizontal transmission hotspots have been identified, and rodents are suggested to be the major retroviral reservoir of type II gammaretroviruses. In addition, by mapping 2 host species onto viral phylogenies, it is shown that cross-species horizontal transmissions of gammaretroviruses are frequent between closely related species. 3 Declaration of Originality I declare that the research presented in this thesis is my own original work. Expect to PCR-derived ERVs from Joanne Martin et al., 2006 (unpublished data) which are included into phylogenetic analyses in Chapter IV. Any additional sources of information have been duly cited in reference list. Copyright Declaration The copyright of this thesis rests with the author and is made available under a Creative Commons Attribution Non-Commercial No Derivatives licence. Researchers are free to copy, distribute or transmit the thesis on the condition that they attribute it, that they do not use it for commercial purposes and that they do not alter, transform or build upon it. For any reuse or redistribution, researchers must make clear to others the licence terms of this work 4 Acknowledgements Foremost, I would like to thank my supervisor, Dr. Michael Tristem, for continuous support of my MSc and PhD Studies, for his patience and immense knowledge. I could not have imagined having a better mentor for my study. My sincere thanks also go to my dear friend and labmate, Dr. Adam Lee, for his encouragement, comments, and music. Also, for all the coffee and fun we had in the last three years. Last but not the least, I would like to thank my parents for giving birth to me at the first place and supporting all my studies in UK. Their love and support have enabled me to learn and grow throughout my years at Imperial College London. My special thanks goes to, Jason Lin, for coming over UK for me, support my life in general, and include me in your life. 5 Table of Contents Title Page…………………………………………………………….….1 Abstract…………………………………………………………….…...2 Declaration of Originality………………………………………………4 Copyright Declaration…………………………………………………..4 Acknowledgements……………………………………………...……...5 Contents Chapter I - Introduction 1.1 Overview and general introduction…………………………………9 1.2 Retroviral genome…………………………………………………14 1.3 Retroviral life cycle……………………………………………..…20 1.4 Retroviral diversity…………………………………………..….…31 1.5 Retroviruses and host genome………………………………….…37 1.6 Evolutionary studies of retroviruses and their hosts………………40 1.7 Co-option of retroviral genes……………………………………...47 Chapter II - A basal retrovirus in an ancient vertebrate lineage 2.1 Introduction………………………………………………………..48 2.2 Materials and Methods…………………………………………….54 2.3 Result………………………………………………………………59 2.3.1 Retroviral distribution in lower vertebrates…………………...59 2.3.2 PmRV, a retrovirus from the Petromyzon marinus genome…..67 2.4 Disucssion 2.4.1 ERV host range and diversity………………………………….83 2.4.2 Genomic organisation analysis of PmRV……………………..88 2.4.3 Putative function for lamprey ERV……………………………94 2.5 Conclusion…………………………………………………………97 Chapter III Evolution of fish retroviruses 3.1 Introduction……………………………………………….……….98 6 3.2 Materials and Methods…………………………………………...100 3.3 Results……………………………………………………………101 3.4 Discussion………………………………………………………..105 3.5 Conclusion………………………………………………………..107 Chapter IV - Biogeographic and horizontal transmission history of mammalian gammaretroviruses 4.1 Introduction………………………………………………...…….108 4.2 Methods and Methods……………………………………...…….112 4.3 Results……………………………………………………………118 4.3.1 Detection and characterization of mammalian gammaretroviruses…………………………………………...118 4.3.2 Gammaretrovirus frequency in mammals……………………134 4.3.3 Rodents are significant vectors of interorder viral transmission events within mammals………………………………………134 4.3.4 Transmission frequency varies according to the genetic distance of donor and recipient………………………………138 4.4 Discussion and Conclusion……………………………………....160 4.4.1 Biogeography and horizontal transmission hotspots of gammaretroviruses………………...…………………………160 4.4.2 Horizontal transmission dynamics of gammaretroviruses…...162 4.4.3 Rodents have more type I gammaretroviruses than other mammals……………………………………………..166 4.4.4 A model of type I mammalian gammaretrovirus evolution….167 Chapter V - Conclusion and Future developments ………………..169 Appendix………...……………………………………………………174 References…………………………………………………………….176 Figure Figure 1.1 11 Figure 1.1.2 13 Figure 1.2.1 16 Figure 1.3.1 21 Figure 1.3.2 23 Figure 1.3.3 25 Figure 1.3.4 26 7 Figure 1.3.5 29 Figure 1.4.1 32 Figure 1.4.2 33 Figure 2.1 50 Figure 2.2 58 Figure 2.3 61 Figure 2.4 67 Figure 2.5 69 Figure 2.6 77 Figure 2.7 80 Figure 2.8 81 Figure 2.9 87 Figure 2.10 88 Figure 2.11 90 Figure 2.12 94 Figure 3.1 104 Figure 4.1 114 Figure 4.2 117 Figure 4.3 119 Figure 4.4 125 Figure 4.5 137 Figure 4.6 139 Figure 4.7 144 Figure 4.8 150 Figure 4.9 151 Figure 4.10 152 Figure 4.11 153 Figure 4.12 154 Figure 4.13 155 Figure 4.14 159 Figure 4.15 163 Figure 4.16 164 Figure 4.17 168 Table Table 1.6.1 44 Table 2.1 55 Table 2.2 90 Table 2.3 96 Table 3.1 103 Table 4.1 118 Table 4.2 135 Table 4.3 158 8 Chapter I Introduction 1.1 Overview and general introduction The Retroviridae is a family of single-stranded positive-sense viruses responsible for many medically important diseases, including immunodeficiencies, sarcomas and leukaemias. Retroviral integration usually occurs in somatic cells. Occasionally, integration occurs in germline cells, resulting in the vertical transmission of retroviruses from parents to offspring (Vogt, 1997). Retroviruses which integrate into host germline cells are termed endogenous retroviruses (ERVs). ERVs may retain the ability to replicate for millions of years and increase in copy number via reinfection or retrotransposition in different locations within the host genome (Sverdlov, 1998). This may result in distinct retrovirus families appearing in host genomes, each originating from a single horizontal interspecies transmission (Tristem, 2000). ERVs could become inactive via recombination deletions and random mutations caused by host DNA replication events (Hughes and Coffin, 2004; Stoye, 2001). At the time of integration, retroviruses contain two identical long terminal repeats (LTRs) at each retroviral terminal (Johnson and Coffin, 1999). Thus, the time of retroviral integration can be estimated from the sequence divergence between the two LTRs, since the divergence should be proportional to the length of time the retroviruses have been subjected to background host mutation. However, the accuracy of this method can be confounded by gene conversion and recombination. Retroviruses can exist in both exogenous and endogenous forms, and some 9 retroviruses can exist in both forms, such as the mouse mammary tumour virus (MMTV) and Jaagsiekte sheep retrovirus (JSRV) (Sarkar et al., 2004; Golovkina et al., 1994; York et al., 1992). ERVs have been isolated in most vertebrates, and the most basal vertebrate in which retroviruses have been identified is the lemon shark (Negaprion brevirostris) (Herniou et al., 1998). Disease-causing retroviruses have been discovered in a range of vertebrates (Vogt, 1997). The first two disease-causing retroviruses discovered, the avian leukaemia virus (ALV) and Rous sarcoma virus (RSV), belong to the alpharetrovirus genus (Rous, 1911; Rous, 1910; Ellerman and Bang, 1909; Ellerman and Bang, 1908). In 1936, the first mammalian retrovirus was discovered in mice, termed mouse mammary tumour virus (MMTV) (Bittner, 1936), which was noticed to be able to transmit murine
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