Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses

Roux, Simon; Enault, François; Bronner, Gisèle; Vaulot, Daniel; Forterre, Patrick; Krupovìč, Mart

doi:10.1038/ncomms3700

Cited by 97 publications

(136 citation statements)

References 69 publications

(106 reference statements)

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“…Thus, the ability of two viruses to exchange their genome segments serves as a general species demarcation criterion. However, our data and other recent observations (87)(88)(89) show that horizontal gene transfer between distantly related viruses plays an important role in viral evolution.…”

Section: Discussioncontrasting

confidence: 43%

“…The acquisition of structural proteins from viruses beyond the family level seems to be rare and is limited to viruses that occupy the same ecological niche and infect the same host. Two recently discovered examples include the transfer of a capsid gene from a ssRNA virus (Tombusviridae) to an ssDNA virus (circo-like virus) (87,88) and the transfer of a capsid from parvoviruses to the Bidnaviridae (89). Reassortment and recombination were for a long time believed to occur only between genetically closely related viruses that show no more than about 5% distance at the nucleotide level (20,(90)(91)(92).…”

Section: Discussionmentioning

confidence: 99%

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A Unique Nodavirus with Novel Features: Mosinovirus Expresses Two Subgenomic RNAs, a Capsid Gene of Unknown Origin, and a Suppressor of the Antiviral RNA Interference Pathway

Schuster

Zirkel

Kurth

et al. 2014

J Virol

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Insects are a reservoir for many known and novel viruses. We discovered an unknown virus, tentatively named mosinovirus (MoNV), in mosquitoes from a tropical rainforest region in Côte d'Ivoire. The MoNV genome consists of two segments of positive-sense RNA of 2,972 nucleotides (nt) (RNA 1) and 1,801 nt (RNA 2). Its putative RNA-dependent RNA polymerase shares 43% amino acid identity with its closest relative, that of the Pariacoto virus (family Nodaviridae). Unexpectedly, for the putative capsid protein, maximal pairwise identity of 16% to Lake Sinai virus 2, an unclassified virus with a nonsegmented RNA genome, was found. Moreover, MoNV virions are nonenveloped and about 50 nm in diameter, larger than any of the known nodaviruses. Mature MoNV virions contain capsid proteins of ϳ56 kDa, which do not seem to be cleaved from a longer precursor. Northern blot analyses revealed that MoNV expresses two subgenomic RNAs of 580 nt (RNA 3) and 292 nt (RNA 4). RNA 4 encodes a viral suppressor of RNA interference (RNAi) that shares its mechanism with the B2 RNAi suppressor protein of other nodaviruses despite lacking recognizable similarity to these proteins. MoNV B2 binds long double-stranded RNA (dsRNA) and, accordingly, inhibits Dicer-2-mediated processing of dsRNA into small interfering RNAs (siRNAs). Phylogenetic analyses indicate that MoNV is a novel member of the family Nodaviridae that acquired its capsid gene via reassortment from an unknown, distantly related virus beyond the family level. IMPORTANCEThe identification of novel viruses provides important information about virus evolution and diversity. Here, we describe an unknown unique nodavirus in mosquitoes, named mosinovirus (MoNV). MoNV was classified as a nodavirus based on its genome organization and on phylogenetic analyses of the RNA-dependent RNA polymerase. Notably, its capsid gene was acquired from an unknown virus with a distant relationship to nodaviruses. Another remarkable feature of MoNV is that, unlike other nodaviruses, it expresses two subgenomic RNAs (sgRNAs). One of the sgRNAs expresses a protein that counteracts antiviral defense of its mosquito host, whereas the function of the other sgRNA remains unknown. Our results show that complete genome segments can be exchanged beyond the species level and suggest that insects harbor a large repertoire of exceptional viruses.

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Section: Discussioncontrasting

confidence: 43%

Section: Discussionmentioning

confidence: 99%

A Unique Nodavirus with Novel Features: Mosinovirus Expresses Two Subgenomic RNAs, a Capsid Gene of Unknown Origin, and a Suppressor of the Antiviral RNA Interference Pathway

Schuster

Zirkel

Kurth

et al. 2014

J Virol

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“…Alternative approaches must therefore be considered for species, genus and perhaps family assignments into the existing ICTV classification. Given the vast numbers and diversity of sequences that are currently generated, particularly of bacteriophages and those with circovirus-like genomes (Roux et al, 2013), it seems that any practical solution would have to bypass the detailed and often timeconsuming information gathering and formal taxonomic assignment procedure used for currently assigned viruses.…”

Section: The Urge To Classifymentioning

confidence: 99%

Methods for virus classification and the challenge of incorporating metagenomic sequence data

Simmonds¹

2015

Journal of General Virology

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The division of viruses into orders, families, genera and species provides a classification framework that seeks to organize and make sense of the diversity of viruses infecting animals, plants and bacteria. Classifications are based on similarities in genome structure and organization, the presence of homologous genes and sequence motifs and at lower levels such as species, host range, nucleotide and antigenic relatedness and epidemiology. Classification below the level of family must also be consistent with phylogeny and virus evolutionary histories. Recently developed methods such as PASC, DEMaRC and NVR offer alternative strategies for genus and species assignments that are based purely on degrees of divergence between genome sequences. They offer the possibility of automating classification of the vast number of novel virus sequences being generated by next-generation metagenomic sequencing. However, distance-based methods struggle to deal with the complex evolutionary history of virus genomes that are shuffled by recombination and reassortment, and where taxonomic lineages evolve at different rates. In biological terms, classifications based on sequence distances alone are also arbitrary whereas the current system of virus taxonomy is of utility precisely because it is primarily based upon phenotypic characteristics. However, a separate system is clearly needed by which virus variants that lack biological information might be incorporated into the ICTV classification even if based solely on sequence relationships to existing taxa. For these, simplified taxonomic proposals and naming conventions represent a practical way to expand the existing virus classification and catalogue our rapidly increasing knowledge of virus diversity.

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“…The latter novel entity, denoted an RNA-DNA hybrid virus (RDHV), probably evolved via a route parallel to that of the evolution of geminiviruses (137). A recent exhaustive analysis of metagenomic sequences led to the discovery of multiple hybrid genomes of putative novel viruses that appear to have evolved via recombination between different groups of positive RNA viruses that provide the CP gene and RCR replicons that are the source of the Rep gene (138).…”

Section: Rolling Circle Replicons: Multiple Transitions From Viruses mentioning

confidence: 99%

Virus World as an Evolutionary Network of Viruses and Capsidless Selfish Elements

Koonin

Dolja

2014

Microbiol Mol Biol Rev

219

211

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SUMMARY Viruses were defined as one of the two principal types of organisms in the biosphere, namely, as capsid-encoding organisms in contrast to ribosome-encoding organisms, i.e., all cellular life forms. Structurally similar, apparently homologous capsids are present in a huge variety of icosahedral viruses that infect bacteria, archaea, and eukaryotes. These findings prompted the concept of the capsid as the virus “self” that defines the identity of deep, ancient viral lineages. However, several other widespread viral “hallmark genes” encode key components of the viral replication apparatus (such as polymerases and helicases) and combine with different capsid proteins, given the inherently modular character of viral evolution. Furthermore, diverse, widespread, capsidless selfish genetic elements, such as plasmids and various types of transposons, share hallmark genes with viruses. Viruses appear to have evolved from capsidless selfish elements, and vice versa, on multiple occasions during evolution. At the earliest, precellular stage of life's evolution, capsidless genetic parasites most likely emerged first and subsequently gave rise to different classes of viruses. In this review, we develop the concept of a greater virus world which forms an evolutionary network that is held together by shared conserved genes and includes both bona fide capsid-encoding viruses and different classes of capsidless replicons. Theoretical studies indicate that selfish replicons (genetic parasites) inevitably emerge in any sufficiently complex evolving ensemble of replicators. Therefore, the key signature of the greater virus world is not the presence of a capsid but rather genetic, informational parasitism itself, i.e., various degrees of reliance on the information processing systems of the host.

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Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses

Cited by 97 publications

References 69 publications

A Unique Nodavirus with Novel Features: Mosinovirus Expresses Two Subgenomic RNAs, a Capsid Gene of Unknown Origin, and a Suppressor of the Antiviral RNA Interference Pathway

A Unique Nodavirus with Novel Features: Mosinovirus Expresses Two Subgenomic RNAs, a Capsid Gene of Unknown Origin, and a Suppressor of the Antiviral RNA Interference Pathway

Methods for virus classification and the challenge of incorporating metagenomic sequence data

Virus World as an Evolutionary Network of Viruses and Capsidless Selfish Elements

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