Ortervirales: New Virus Order Unifying Five Families of Reverse-Transcribing Viruses

Krupovìč, Mart; Blomberg, Jonas; Coffin, John M.; Dasgupta, Indranil; Fan, Hung; Geering, Andrew D. W.; Gifford, Robert J.; Harrach, Balázs; Hull, Roger; Johnson, Welkin E.; Kreuze, Jan; Lindemann, Dirk; Lloréns, Carlos; Lockhart, Benham E; Mayer, Jens; Muller, Emmanuelle; Olszewski, Neil E.; Pappu, H. R.; Pooggin, Mikhail M.; Richert-Pöggeler, Katja; Sabanadzovic, Sead; Sanfaçon, Hélène; Schoelz, James E.; Seal, Susan; Stavolone, Livia; Stoye, Jonathan P.; Teycheney, Pierre‐Yves; Tristem, Michael; Koonin, Eugene V.; Kuhn, Jens H.

doi:10.1128/jvi.00515-18

Cited by 86 publications

(80 citation statements)

References 28 publications

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“…More specifically, the highest similarity is observed between the +RNA virus RdRps and the RTs of group II introns. These introns are wide-spread retrotransposons in prokaryotes that are thought to be ancestral to the RTs of all other retrotransposons as well as retroviruses and pararetroviruses (recently jointly classified as the order Ortervirales) of eukaryotes (27-30).…”

Section: Introductionmentioning

confidence: 99%

Origins and Evolution of the Global RNA Virome

Dolja¹,

Wolf

Kazlauskas³

et al. 2018

Preprint

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116

196

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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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Section: Introductionmentioning

confidence: 99%

Origins and Evolution of the Global RNA Virome

Dolja¹,

Wolf

Kazlauskas³

et al. 2018

Preprint

Self Cite

116

196

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“…Saccharomyces genomes contain many long terminal repeats (LTR) retrotransposons of the Ty1/copia (Ty1, Ty2, Ty4 and Ty5) and Ty3/gypsy Ty3families. Ty1/copia and Ty3/gypsy retrotransposon superfamilies (Wicker et al, 2007) respectively correspond to the Pseudoviridae and Metaviridae virus families (Krupovic et al, 2018) and have a broad taxonomic distribution. Ty elements comprise two overlapping open reading frames (ORFs) within a ~5 kb internal sequence, which is flanked by two ~300 bp LTRs in direct orientation.…”

Section: Introductionmentioning

confidence: 99%

The effect of hybridization on transposable element accumulation in an undomesticated fungal species

Hénault

Marsit

Charron

et al. 2020

Preprint

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Transposable elements (TEs) are mobile genetic elements that can profoundly impact the evolution of genomes and species. A long-standing hypothesis suggests that the merging of diverged genomes within hybrids could alter the regulation of TEs and increase transposition.Higher transposition rates could potentially fuel hybrid evolution with rare adaptive TE insertions, but also cause postzygotic reproductive isolation if maladaptive insertion loads render hybrids sterile or inviable. Mixed evidence for higher TE activity in hybrids was reported in many animal and plant species. Here, we tested for increased TE accumulation in hybrids between incipient species of the undomesticated yeast Saccharomyces paradoxus. Population genomic data revealed no increase in TE content in the natural hybrid lineages. As we could not rule out the elimination of past transposition increase signatures by natural selection, we performed a laboratory evolution experiment on a panel of artificial hybrids to measure TE accumulation in controlled conditions and in the near absence of selection. Changes in TE copy numbers were highly dependent on the individual hybrid genotypes and were not predicted by the evolutionary divergence between the parents of a hybrid genotype. Rather, our data suggested that initial TE copy numbers in hybrids negatively impacted transposition rate, suggesting that TE self-regulation could play a predominant role on TE accumulation in yeast hybrids.

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“…Researchers have yet to observe integrated HIV-1 in one take, hindering locusspecific studies. Complicating matters is the cycling that all orterviruses [1] undergo between two major states (as infectious virion RNA and integrated proviral DNA), repetitive viral sequences like long terminal repeats (LTRs), non-integrated forms [2], and alternative splicing of viral mRNAs [3]. Short read DNA sequencing (less than 150 base pairs (bp) in most reported experiments, but up to 500 bp) provides some information, but analyses require high coverage and extensive effort (non-exhaustive examples [4,5]).…”

Section: Introductionmentioning

confidence: 99%

Reference plasmid pHXB2_D is an HIV-1 molecular clone that exhibits identical LTRs and a single integration site indicative of an HIV provirus

Gener

2019

Preprint

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Objective(s):To evaluate nanopore DNA sequencing for sequencing full-length HIV-1 provirus.Design: I used nanopore sequencing to sequence full-length HIV-1 from a plasmid (pHXB2).Methods: pHXB2 plasmid was processed with the Rapid PCR-Barcoding library kit and sequenced on the MinION sequencer (Oxford Nanopore Technologies, Oxford., UK). Raw fast5 reads were converted into fastq (base called) with Albacore, Guppy, and FlipFlop base callers. Reads were first aligned to the reference with BWA-MEM to evaluate sample coverage manually. Reads were then assembled with Canu into contigs, and contigs manually finished in SnapGene.Results: I sequenced full-length HXB2 HIV-1 from 5' to 3' LTR (100%), with median perbase coverage of over 9000x in one 12-barcoded experiment on a single MinION flow cell.The longest HIV-spanning read to-date was generated, at a length of 11,487 bases, which included full-length HIV-1 and plasmid backbone on either side. At least 20 variants were discovered in pHXB2 compared to reference. Conclusions:The MinION sequencer performed as-expected, covering full-length HIV. The discovery of variants in a dogmatic reference plasmid demonstrates the need for singlemolecule sequence verification moving forward. These results illustrate the utility of long read sequencing to advance the study of HIV at single integration site resolution.

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Ortervirales: New Virus Order Unifying Five Families of Reverse-Transcribing Viruses

Cited by 86 publications

References 28 publications

Origins and Evolution of the Global RNA Virome

Origins and Evolution of the Global RNA Virome

The effect of hybridization on transposable element accumulation in an undomesticated fungal species

Reference plasmid pHXB2_D is an HIV-1 molecular clone that exhibits identical LTRs and a single integration site indicative of an HIV provirus

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