Endogenous Viral Elements in Shrew Genomes Provide Insights into <i>Pestivirus</i> Ancient History

Li, Yiqiao; Bletsa, Magda; Zisi, Zafeiro; Boonen, Ine; Gryseels, Sophie; Kafetzopoulou, LE; Webster, Joanne P.; Catalano, Stefano; Pybus, Oliver G.; Perre, Frederik Van de; Ht, Li; Li, Yuanyuan; Yc, Li; Abramov, Alexei V.; Lymberakis, Petros; Lemey, Philippe; Lequime, Sébastian

doi:10.1093/molbev/msac190

Cited by 11 publications

(11 citation statements)

References 91 publications

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“…While CnidFV and the peach blossom jellyfish EVE are relatively closely related to each other, there is substantial genetic divergence between these sequences. This has been previously observed with crocidura pestivirus and a Crocidura EVE and may reflect divergent evolution since the historic endogenization event ( Li et al. 2022 ).…”

Section: Discussionsupporting

confidence: 69%

Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians

et al. 2022

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The flavivirids (family Flaviviridae) are a group of positive-sense RNA viruses that include well-documented agents of human disease. Despite their importance and ubiquity, the time-scale of flavivirid evolution is uncertain. An ancient origin, spanning millions of years, is supported by their presence in both vertebrates and invertebrates and by the identification of a flavivirus-derived endogenous viral element in the peach blossom jellyfish genome (Craspedacusta Sowerby, phylum Cnidaria), implying that the flaviviruses arose early in the evolution of the Metazoa. To date, however, no exogenous flavivirid sequences have been identified in these hosts. To help resolve the antiquity of the Flaviviridae, we mined publicly available transcriptome data across the Metazoa. From this, we expanded the diversity within the family through the identification of 32 novel viral sequences and extended the host range of the pestiviruses to include amphibians, reptiles, and ray-finned fish. Through cophylogenetic analysis we found cross-species transmission to be the predominate macroevolutionary event across the non-vectored flavivirid genera (median, 68%), including a cross-species transmission event between bats and rodents, although long-term virus-host co-divergence was still a regular occurrence (median, 23%). Notably, we discovered flavivirus-like sequences in basal metazoan species, including the first associated with Cnidaria. This sequence formed a basal lineage to the genus Flavivirus and was closer to arthropod and crustacean flaviviruses than those in the tamanavirus group that include a variety of invertebrate and vertebrate viruses. Combined, these data attest an ancient origin of the flaviviruses, likely close to the emergence of the metazoans 750–800 million years ago.

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Section: Discussionsupporting

confidence: 69%

Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians

et al. 2022

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“…The only examples we identified were a small number of sequences derived from flavivirids (family Flaviviridae ). These include an EVE derived from the Pestivirus genus of flavivirids, the reference genome of the Indochinese shrew ( Crocidura indochinensis ), as reported previously [56], and EVEs identified in ray-finned fish, also reported previously [57]. In fish genomes, flavivirid EVEs derive from the proposed ‘Tamanavirus’ genus, and a lineage labelled ‘X2’ that groups as a sister taxon to the proposed ‘Jingmenvirus’ genus.…”

Section: Resultssupporting

confidence: 57%

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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“…While CnidFV and the EVE are relatively closely related to each other, there is a large amount of divergence between these sequences. This has been previously observed with crocidura pestivirus and a Crocidura EVE and may reflect divergent evolution since the historic endogenization event (Li et al 2022).…”

Section: Discussionsupporting

confidence: 67%

Transcriptome mining extends the host range of theFlaviviridaeto non-bilaterians

Mifsud

Costa

Petrone

et al. 2022

Preprint

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The Flaviviridae are a family of positive-sense RNA viruses that include well documented agents of human disease. Despite their importance and ubiquity, the timescale of flaviviral evolution is uncertain. An ancient origin, spanning timescales of millions of years, is supported by their presence in both vertebrates and invertebrates and the identification of a flavivirus derived endogenous viral element in the peach blossom jellyfish genome (Craspedacusta Sowerby, phylum Cnidaria), implying that the flaviviruses arose early in the evolution of the Metazoa. To date, however, no exogenous flavivirus sequences have been identified in these hosts. To help resolve the antiquity of the Flavivirdae we mined publicly available transcriptome data across the Metazoa. From this, we expanded the diversity within the family through the identification of 32 novel viral sequences, and extended the host range of the pestiviruses to include amphibians, reptiles, and ray-finned fish. Through co-phylogenetic analysis we found cross-species transmission to be the predominate macroevolutionary event across the non-vectored flaviviral genera (median, 68%), including a cross-species transmission event between bats and rodents, although long-term virus-host co-divergence was still a regular occurrence (median, 23%). Notably, we discovered flavivirus-like sequences in basal metazoan species, including the first associated with Cnidaria. This sequence formed a basal lineage to the genus Flavivirus and was closer to arthropod and crustacean flaviviruses than those in the tamanavirus group that include a variety of invertebrate and vertebrate viruses. Combined, these data attest an ancient origin of the flaviviruses, close to the emergence of the metazoans 750-800 million years ago.

show abstract

Endogenous Viral Elements in Shrew Genomes Provide Insights into Pestivirus Ancient History

Cited by 11 publications

References 91 publications

Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians

Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians

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

Transcriptome mining extends the host range of theFlaviviridaeto non-bilaterians

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