Evolutionary biology of members of the viral kingdom Bamfordvirae
Members of the viral kingdom Bamfordvirae arguably represent the most diverse lineage of viruses infecting eukaryotes. They comprise the Nucleocytoplasmic Large DNA viruses (NCLDVs), virophages, adenoviruses, Maverick/Polintons and Polinton-like viruses. Most elements encode a conserved module of ge...
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| Format: | Thesis |
| Language: | English |
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2022
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| _version_ | 1797111594821353472 |
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| author | Niño Barreat, JG |
| author2 | Katzourakis, A |
| author_facet | Katzourakis, A Niño Barreat, JG |
| author_sort | Niño Barreat, JG |
| collection | OXFORD |
| description | Members of the viral kingdom Bamfordvirae arguably represent the most diverse lineage of viruses infecting eukaryotes. They comprise the Nucleocytoplasmic Large DNA viruses (NCLDVs), virophages, adenoviruses, Maverick/Polintons and Polinton-like viruses. Most elements encode a conserved module of genes involved in capsid formation: two jelly-roll fold capsid proteins, an FtsK-HerA DNA-packaging ATPase and an adenoviral-like protease. However, over the course of evolution, these viruses diversified to an unprecedented extent by numerous gene gains and losses, replacement of the ancestral replicase and acquisition of integrases. I investigated aspects of the evolutionary biology of this viral kingdom by combining results from paleovirology, phylogenetics, mathematical modelling and computational simulations. First, I show that Mavericks have undergone frequent cross-species transmissions and the genes involved in capsid formation are under strong purifying selection. These observations imply that Mavericks are endogenous viruses and not merely transposons. Maverick viruses were estimated to have infected vertebrates for at least 419 million years. Next, I found support for an alternative evolutionary scenario for the origin of the bamfordviruses of eukaryotes, which is at odds with the nuclear-escape hypothesis (origin from a Maverick-like element that escaped from the nucleus). The topology of the phylogenetic tree suggests that this viral lineage has infected eukaryotes for > 1 billion years. By modelling the interactions between cells, viruses and virophages, I argue that the virophage entry mechanism is potentially the main driver of the different integration patterns observed for Mavirus/Spuntik-like virophages. Theoretical analyses also supported the role of virophage inhibition, programmed cell-death and multicellularity as effective antiviral mechanisms in microbial eukaryotes. Finally, I explored the evolutionary biology of two Maverick integrations found in the human genome, which integrated at least ~102 million years ago. These results shed light on the ancient interactions of viruses with eukaryotes, and present new questions and hypotheses open for investigation. |
| first_indexed | 2024-03-07T08:11:03Z |
| format | Thesis |
| id | oxford-uuid:63d315f9-2462-43bb-b3f6-6b4670caa46b |
| institution | University of Oxford |
| language | English |
| last_indexed | 2024-03-07T08:11:03Z |
| publishDate | 2022 |
| record_format | dspace |
| spelling | oxford-uuid:63d315f9-2462-43bb-b3f6-6b4670caa46b2023-11-29T07:19:29ZEvolutionary biology of members of the viral kingdom BamfordviraeThesishttp://purl.org/coar/resource_type/c_db06uuid:63d315f9-2462-43bb-b3f6-6b4670caa46bVirologyZoologyEvolutionComputer simulationMathematical modelsComparative genomicsEnglishHyrax Deposit2022Niño Barreat, JGKatzourakis, AMembers of the viral kingdom Bamfordvirae arguably represent the most diverse lineage of viruses infecting eukaryotes. They comprise the Nucleocytoplasmic Large DNA viruses (NCLDVs), virophages, adenoviruses, Maverick/Polintons and Polinton-like viruses. Most elements encode a conserved module of genes involved in capsid formation: two jelly-roll fold capsid proteins, an FtsK-HerA DNA-packaging ATPase and an adenoviral-like protease. However, over the course of evolution, these viruses diversified to an unprecedented extent by numerous gene gains and losses, replacement of the ancestral replicase and acquisition of integrases. I investigated aspects of the evolutionary biology of this viral kingdom by combining results from paleovirology, phylogenetics, mathematical modelling and computational simulations. First, I show that Mavericks have undergone frequent cross-species transmissions and the genes involved in capsid formation are under strong purifying selection. These observations imply that Mavericks are endogenous viruses and not merely transposons. Maverick viruses were estimated to have infected vertebrates for at least 419 million years. Next, I found support for an alternative evolutionary scenario for the origin of the bamfordviruses of eukaryotes, which is at odds with the nuclear-escape hypothesis (origin from a Maverick-like element that escaped from the nucleus). The topology of the phylogenetic tree suggests that this viral lineage has infected eukaryotes for > 1 billion years. By modelling the interactions between cells, viruses and virophages, I argue that the virophage entry mechanism is potentially the main driver of the different integration patterns observed for Mavirus/Spuntik-like virophages. Theoretical analyses also supported the role of virophage inhibition, programmed cell-death and multicellularity as effective antiviral mechanisms in microbial eukaryotes. Finally, I explored the evolutionary biology of two Maverick integrations found in the human genome, which integrated at least ~102 million years ago. These results shed light on the ancient interactions of viruses with eukaryotes, and present new questions and hypotheses open for investigation. |
| spellingShingle | Virology Zoology Evolution Computer simulation Mathematical models Comparative genomics Niño Barreat, JG Evolutionary biology of members of the viral kingdom Bamfordvirae |
| title | Evolutionary biology of members of the viral kingdom Bamfordvirae |
| title_full | Evolutionary biology of members of the viral kingdom Bamfordvirae |
| title_fullStr | Evolutionary biology of members of the viral kingdom Bamfordvirae |
| title_full_unstemmed | Evolutionary biology of members of the viral kingdom Bamfordvirae |
| title_short | Evolutionary biology of members of the viral kingdom Bamfordvirae |
| title_sort | evolutionary biology of members of the viral kingdom bamfordvirae |
| topic | Virology Zoology Evolution Computer simulation Mathematical models Comparative genomics |
| work_keys_str_mv | AT ninobarreatjg evolutionarybiologyofmembersoftheviralkingdombamfordvirae |