A Novel Bunyavirus-Like Virus of Trypanosomatid Protist Parasites

Akopyants, Natalia S.; Lye, Lon-Fye; Dobson, Deborah E.; Lukeš, J; Beverley, Stephen M.

doi:10.1128/genomea.00715-16

Cited by 26 publications

(30 citation statements)

References 8 publications

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“…Instead, branches 4 and 5 are separate and positioned deep in the tree, immediately above the split between branch 1 and the rest of the RdRps. Given the poor resolution of the RAxML tree and a strong biological argument, namely, the absence of identified ϪRNA viruses in prokaryotes or protists (with the exception of the "leishbuviruses" infecting kinetoplastids [49,50]; see also Discussion below), we believe that the tree topology presented in Fig. 1 carries more credence than that shown in Data Set S3B.…”

Section: Resultsmentioning

confidence: 90%

“…In land plants, RNA viruses, particularly those of branch 3, dramatically expanded, perhaps in part because of the exclusion of competing large DNA viruses. Finally, it seems plausible that, given the high prevalence of ϪRNA viruses in metazoa and their virtual absence in protists (with the exception of the recently discovered "leishbuviruses" that likely invaded their parasitic protist hosts via HVT from an animal host [49,50]), the viruses that comprise RdRp branch 5 evolved in animals via mixing and matching genes from reovirus-like and flavivirus-like ancestors.…”

Section: Discussionmentioning

confidence: 99%

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Origins and Evolution of the Global RNA Virome

Wolf

Kazlauskas

Iranzo

et al. 2018

mBio

444

333

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Viruses with RNA genomes dominate the eukaryotic virome, reaching enormous diversity in animals and plants. The recent advances of metaviromics prompted us to perform a detailed phylogenomic reconstruction of the evolution of the dramatically expanded global RNA virome. The only universal gene among RNA viruses is the gene encoding the RNA-dependent RNA polymerase (RdRp). We developed an iterative computational procedure that alternates the RdRp phylogenetic tree construction with refinement of the underlying multiple-sequence alignments. The resulting tree encompasses 4,617 RNA virus RdRps and consists of 5 major branches; 2 of the branches include positive-sense RNA viruses, 1 is a mix of positive-sense (ϩ) RNA and double-stranded RNA (dsRNA) viruses, and 2 consist of dsRNA and negative-sense (Ϫ) RNA viruses, respectively. This tree topology implies that dsRNA viruses evolved from ϩRNA viruses on at least two independent occasions, whereas ϪRNA viruses evolved from dsRNA viruses. Reconstruction of RNA virus evolution using the RdRp tree as the scaffold suggests that the last common ancestors of the major branches of ϩRNA viruses encoded only the RdRp and a single jelly-roll capsid protein. Subsequent evolution involved independent capture of additional genes, in particular, those encoding distinct RNA helicases, enabling replication of larger RNA genomes and facilitating virus genome expression and virus-host interactions. Phylogenomic analysis reveals extensive gene module exchange among diverse viruses and horizontal virus transfer between distantly related hosts. Although the network of evolutionary relationships within the RNA virome is bound to further expand, the present results call for a thorough reevaluation of the RNA virus taxonomy. IMPORTANCE The majority of the diverse viruses infecting eukaryotes have RNA genomes, including numerous human, animal, and plant pathogens. Recent advances of metagenomics have led to the discovery of many new groups of RNA viruses in a wide range of hosts. These findings enable a far more complete reconstruction of the evolution of RNA viruses than was attainable previously. This reconstruction reveals the relationships between different Baltimore classes of viruses and indicates extensive transfer of viruses between distantly related hosts, such as plants and animals. These results call for a major revision of the existing taxonomy of RNA viruses.

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Section: Resultsmentioning

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Origins and Evolution of the Global RNA Virome

Wolf

Kazlauskas

Iranzo

et al. 2018

mBio

444

333

View full text Add to dashboard Cite

show abstract

“…Instead, Branches 4 and 5 are separate and positioned deep in the tree, right above the split between Branch 1 and the rest of the RdRps. Given the poor resolution of the RAxML tree and a strong biological argument, namely, the absence of identified-RNA viruses in prokaryotes or protists (with the exception of the “leishbuviruses” infecting kinetoplastids (49, 50); see also discussion below), we believe that the tree topology in Figure 1 carries more credence than that shown in Data set S3B. Nevertheless, these discrepancies emphasize that utmost caution is due when biological interpretation of deep branching in trees of highly divergent proteins is attempted.…”

Section: Resultsmentioning

confidence: 99%

“…In land plants, RNA viruses, particularly those of Branch 3, dramatically expanded, in part, perhaps, because of the exclusion of competing large DNA viruses. Finally, it seems plausible that, given the high prevalence of-RNA viruses in metazoa and their virtual absence in protists [with the exception of the recently discovered “leishbuviruses” that likely invaded their parasitic protist hosts via HVT from an animal host (49, 50)], these viruses that comprise the RdRp Branch 5 evolved in animals via mixing and matching genes from reovirus-like and flavivirus-like ancestors.…”

Section: Discussionmentioning

confidence: 99%

Origins and Evolution of the Global RNA Virome

Dolja¹,

Wolf

Kazlauskas³

et al. 2018

Preprint

118

197

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Viruses with RNA genomes dominate the eukaryotic virome, reaching enormous diversity in animals and plants. The recent advances of metaviromics prompted us to perform a detailed phylogenomic reconstruction of the evolution of the dramatically expanded global RNA virome. The only universal gene among RNA viruses is the RNA-dependent RNA polymerase (RdRp). We developed an iterative computational procedure that alternates the RdRp phylogenetic tree construction with refinement of the underlying multiple sequence alignments. The resulting tree encompasses 4,617 RNA virus RdRps and consists of 5 major branches, 2 of which include positive-sense RNA viruses, 1 is a mix of positive-sense (+) RNA and double-stranded (ds) RNA viruses, and 2 consist of dsRNA and negative-sense (−) RNA viruses, respectively. This tree topology implies that dsRNA viruses evolved from +RNA viruses on at least two independent occasions, whereas -RNA viruses evolved from dsRNA viruses. Reconstruction of RNA virus evolution using the RdRp tree as the scaffold suggests that the last common ancestors of the major branches of +RNA viruses encoded only the RdRp and a single jelly-roll capsid protein. Subsequent evolution involved independent capture of additional genes, particularly, those encoding distinct RNA helicases, enabling replication of larger RNA genomes and facilitating virus genome expression and virus-host interactions. Phylogenomic analysis reveals extensive gene module exchange among diverse viruses and horizontal virus transfer between distantly related hosts. Although the network of evolutionary relationships within the RNA virome is bound to further expand, the present results call for a thorough reevaluation of the RNA virus taxonomy.IMPORTANCEThe majority of the diverse viruses infecting eukaryotes have RNA genomes, including numerous human, animal, and plant pathogens. Recent advances of metagenomics have led to the discovery of many new groups of RNA viruses in a wide range of hosts. These findings enable a far more complete reconstruction of the evolution of RNA viruses than what was attainable previously. This reconstruction reveals the relationships between different Baltimore Classes of viruses and indicates extensive transfer of viruses between distantly related hosts, such as plants and animals. These results call for a major revision of the existing taxonomy of RNA viruses.

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“…Given such a complexity of host structure, combined with still very sparse sampling, it is dangerous to construct detailed ancestor-descendant relationships on the currently available data. For example, arthropods were initially proposed to be the ancestral hosts of bunyaviruses (Marklewitz et al, 2015), although more divergent viruses in this group have now been discovered in other invertebrates, fungi, and protists (Akopyants et al, 2016;Shi et al, 2016a).…”

Section: Cross-species Transmission and Emergencementioning

confidence: 99%

Meta-transcriptomics and the evolutionary biology of RNA viruses

2018

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Metagenomics is transforming the study of virus evolution, allowing the full assemblage of virus genomes within a host sample to be determined rapidly and cheaply. The genomic analysis of complete transcriptomes, so-called meta-transcriptomics, is providing a particularly rich source of data on the global diversity of RNA viruses and their evolutionary history. Herein we review some of the insights that meta-transcriptomics has provided on the fundamental patterns and processes of virus evolution, with a focus on the recent discovery of a multitude of novel invertebrate viruses. In particular, meta-transcriptomics shows that the RNA virus world is more fluid than previously realized, with relatively frequent changes in genome length and structure. As well as having a transformative impact on studies of virus evolution, meta-transcriptomics presents major new challenges for virus classification, with the greater sampling of host taxa now filling many of the gaps on virus phylogenies that were previously used to define taxonomic groups. Given that most viruses in the future will likely be characterized using metagenomics approaches, and that we have evidently only sampled a tiny fraction of the total virosphere, we suggest that proposals for virus classification pay careful attention to the wonders unearthed in this new age of virus discovery.

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A Novel Bunyavirus-Like Virus of Trypanosomatid Protist Parasites

Cited by 26 publications

References 8 publications

Origins and Evolution of the Global RNA Virome

Origins and Evolution of the Global RNA Virome

Origins and Evolution of the Global RNA Virome

Meta-transcriptomics and the evolutionary biology of RNA viruses

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