Comparative analysis of genome-encoded viral sequences reveals the evolutionary history of flavivirids (family <i>Flaviviridae</i>)

Bamford, Connor; Souza, William Marciel de; Parry, Rhys; Gifford, Robert J.

doi:10.1093/ve/veac085

Cited by 21 publications

(34 citation statements)

References 68 publications

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“…Using this alignment, we reconstructed a consensus maximum-likelihood phylogenetic tree using IQ-TREE2 (). The resultant phylogenetic trees were robustly supported with reasonable bootstrap support values, and this tree’s overall topology is congruent with previously created phylogenies [3, 4]. RaTV clusters basally to a clade that encompasses CuLV and TABV.…”

Section: Resultssupporting

confidence: 77%

“…Flavivirids (family Flaviviridae) are small enveloped viruses with a positive sense (+), monopartite RNA genome between ~9 and 13 kb in length and encompass the genera Flavivirus, Pestivirus, Pegivirus and Hepacivirus [2]. Flavivirids have a long evolutionary history and co-divergence with metazoans, with estimates of time scales in the hundreds of millions of years [3][4][5].…”

Section: Introductionmentioning

confidence: 99%

“…Despite sharing conserved protein domain architecture, these flavi-like sequences do not form a monophyletic grouping with the four established groups of flaviviruses, instead representing a basal group to all flaviviruses. These viruses are collectively referred to as tamanaviruses in recent publications [3,14], named after the prototype species Tamana bat virus (TABV), which was isolated from Pteronotus parnellii, an insectivorous bat known as Parnell's moustached bat [15,16].…”

mentioning

confidence: 99%

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A novel tamanavirus (Flaviviridae) of the European common frog (Rana temporaria) from the UK

Parry,

Slonchak,

Campbell

et al. 2023

Journal of General Virology

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Flavivirids are small, enveloped, positive-sense RNA viruses from the family Flaviviridae with genomes of ~9–13 kb. Metatranscriptomic analyses of metazoan organisms have revealed a diversity of flavivirus-like or flavivirid viral sequences in fish and marine invertebrate groups. However, no flavivirus-like virus has been identified in amphibians. To remedy this, we investigated the virome of the European common frog (Rana temporaria) in the UK, utilizing high-throughput sequencing at six catch locations. De novo assembly revealed a coding-complete virus contig of a novel flavivirid ~11.2 kb in length. The virus encodes a single ORF of 3456 aa and 5′ and 3′ untranslated regions (UTRs) of 227 and 666 nt, respectively. We named this virus Rana tamanavirus (RaTV), as BLASTp analysis of the polyprotein showed the closest relationships to Tamana bat virus (TABV) and Cyclopterus lumpus virus from Pteronotus parnellii and Cyclopterus lumpus, respectively. Phylogenetic analysis of the RaTV polyprotein compared to Flavivirus and Flavivirus-like members indicated that RaTV was sufficiently divergent and basal to the vertebrate Tamanavirus clade. In addition to the Mitcham strain, partial but divergent RaTV, sharing 95.64–97.39 % pairwise nucleotide identity, were also obtained from the Poole and Deal samples, indicating that RaTV is widespread in UK frog samples. Bioinformatic analyses of predicted secondary structures in the 3′UTR of RaTV showed the presence of an exoribonuclease-resistant RNA (xrRNA) structure standard in flaviviruses and TABV. To examine this biochemically, we conducted an in vitro Xrn1 digestion assay showing that RaTV probably forms a functional Xrn1-resistant xrRNA.

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Section: Resultssupporting

confidence: 77%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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A novel tamanavirus (Flaviviridae) of the European common frog (Rana temporaria) from the UK

Parry,

Slonchak,

Campbell

et al. 2023

Journal of General Virology

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“…The final component denotes the taxonomic distribution of the element. This approach has been applied in several previous studies of vertebrate EVEs [47, 48, 50, 57]. Where appropriate, we maintained consistency with previous studies.…”

Section: Methodsmentioning

confidence: 88%

A novel approach to exploring the dark genome and its application to mapping of the vertebrate virus ‘fossil record’

Blanco-Melo,

Campbell,

Zhu

et al. 2023

Preprint

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Background: Genomic regions that remain poorly understood, often referred to as the "dark genome," contain a variety of functionally relevant and biologically informative genome features. These include endogenous viral elements (EVEs) - virus-derived sequences that can dramatically impact host biology and serve as a virus "fossil record". In this study, we introduce a database-integrated genome screening (DIGS) approach to investigating the dark genome in silico, focusing on EVEs found within vertebrate genomes. Results: Using DIGS on 874 vertebrate species genomes, we uncovered approximately 1.1 million EVE sequences, with over 99% originating from endogenous retroviruses or transposable elements that contain EVE DNA. We show that the remaining 6038 sequences represent over a thousand distinct horizontal gene transfer events across ten virus families, including some that have not previously been reported as EVEs. We explore the genomic and phylogenetic characteristics of non-retroviral EVEs and determine their rates of acquisition during vertebrate evolution. Our study uncovers novel virus diversity and broadens our knowledge of virus distribution among vertebrate hosts. It also provides new insights into the long-term evolution of highly pathogenic filoviruses. Conclusions: We comprehensively catalogue and analyse EVEs within 874 vertebrate genomes, shedding light on the distribution, diversity and long-term evolution of viruses, and revealing their extensive impact on vertebrate genome evolution. Our results demonstrate the power of linking a relational database management system to a similarity search-based screening pipeline for in silico exploration of the dark genome.

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“…For example, members of the family Flaviviridae (single-strand positive-sense RNA viruses) were recently discovered in basal invertebrates (Cnidaria) 13 , basal chordates (Ascidia) 13 , and in diverse aquatic environments 14 . This suggests that the Flaviviridae , which include such human pathogens as dengue virus and yellow fever virus, emerged concurrently with the origin of the Metazoa (i.e., animals) some 750-800 million years ago 15 . Indeed, that aquatic ecosystems may have influenced the evolution of terrestrial viruses speaks both to the virus diversity these environments support and to their role as the source of life on Earth.…”

Section: Introductionmentioning

confidence: 99%

Evidence for an aquatic origin of influenza virus and the orderArticulavirales

Parry

Mifsud

et al. 2023

Preprint

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The emergence of novel disease-causing viruses in mammals is part of the long evolutionary history of viruses. Tracing these evolutionary histories contextualises virus spill over events and may help to elucidate how and why they occur. We used a combination of total RNA sequencing and transcriptome data mining to extend the diversity and evolutionary history of the order Articulavirales, which includes the influenza viruses. From this, we identified the first instance of Articulavirales in the Cnidaria (including corals), constituting a novel and divergent family that we tentatively named the Cnidenomoviridae. This may be the basal group within the Articulavirales. We also extended the known evolutionary history of the influenza virus lineage by identifying a highly divergent, sturgeon-associated influenza virus. This suggests that fish were among the first hosts of influenza viruses. Finally, we substantially expanded the known diversity of quaranjaviruses and proposed that this genus be reclassified as a family (the Quaranjaviridae). We find evidence that vertebrate infecting Quaranjaviridae may have initially evolved in crustaceans before spilling into terrestrial Chelicerata (i.e., ticks). Together, our findings indicate that the Articulavirales has evolved over at least 600 million years, first emerging in aquatic animals. Importantly, the evolution of this order was not shaped by strict virus-host codivergence, but rather by multiple aquatic-terrestrial transitions and substantial host jumps, some of which are still observable today.

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Comparative analysis of genome-encoded viral sequences reveals the evolutionary history of flavivirids (family Flaviviridae)

Cited by 21 publications

References 68 publications

A novel tamanavirus (Flaviviridae) of the European common frog (Rana temporaria) from the UK

A novel tamanavirus (Flaviviridae) of the European common frog (Rana temporaria) from the UK

A novel approach to exploring the dark genome and its application to mapping of the vertebrate virus ‘fossil record’

Evidence for an aquatic origin of influenza virus and the orderArticulavirales

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