A case for a reverse-frame coding sequence in a group of positive-sense RNA viruses

Dinan, Adam M.; Lukhovitskaya, Nina I.; Olendraitė, Ingrida; Firth, Andrew E.

doi:10.1101/664342

Cited by 33 publications

(73 citation statements)

References 72 publications

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“…representing 99% of all assigned contigs, makes it likely that most if not all of these 18 viruses infect algae hosts. In addition, we identified a number of narnaviruses, a group previously observed in algae [ 69 , 70 ], and our observation of a Bunyavirales -like sequence is similarly in accord with a study that presented evidence for the presence of bunya/phlebo-like viruses in brown algae [ 71 ]. As such, the apparent domination of DNA viruses in microalgae at least partially reflects major sampling biases.…”

Section: Discussionsupporting

confidence: 89%

Metatranscriptomic Identification of Diverse and Divergent RNA Viruses in Green and Chlorarachniophyte Algae Cultures

Charon

Marcelino

Wetherbee

et al. 2020

Viruses

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Our knowledge of the diversity and evolution of the virosphere will likely increase dramatically with the study of microbial eukaryotes, including the microalgae within which few RNA viruses have been documented. By combining total RNA sequencing with sequence and structural-based homology detection, we identified 18 novel RNA viruses in cultured samples from two major groups of microbial algae: the chlorophytes and the chlorarachniophytes. Most of the RNA viruses identified in the green algae class Ulvophyceae were related to the Tombusviridae and Amalgaviridae viral families commonly associated with land plants. This suggests that the evolutionary history of these viruses extends to divergence events between algae and land plants. Seven Ostreobium sp-associated viruses exhibited sequence similarity to the mitoviruses most commonly found in fungi, compatible with horizontal virus transfer between algae and fungi. We also document, for the first time, RNA viruses associated with chlorarachniophytes, including the first negative-sense (bunya-like) RNA virus in microalgae, as well as a distant homolog of the plant virus Virgaviridae, potentially signifying viral inheritance from the secondary chloroplast endosymbiosis that marked the origin of the chlorarachniophytes. More broadly, these data suggest that the scarcity of RNA viruses in algae results from limited investigation rather than their absence.

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Section: Discussionsupporting

confidence: 89%

Metatranscriptomic Identification of Diverse and Divergent RNA Viruses in Green and Chlorarachniophyte Algae Cultures

Charon

Marcelino

Wetherbee

et al. 2020

Viruses

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“…1B ). We did not find any degree of conservation aligning the rORF of the nine narnaviruses (PVaNarna15, 22, 23, 24, 25, 26, 41, 42, and 43) as already shown for other ambisense narnaviruses ( Dinan et al. 2020 ).…”

Section: Resultssupporting

confidence: 70%

Analysis of the virome associated to grapevine downy mildew lesions reveals new mycovirus lineages

et al. 2020

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The obligatory biotrophic oomycetes Plasmopara viticola is the causal agent of downy mildew, a destructive disease of grapevine worldwide. So far, chemical fungicides are widely employed to limit this pathogen, but their adverse effects are stimulating the quest for environmentally friendly alternative approaches. Here we report on the search for mycoviruses that might be later developed as biocontrol agents for this pathogen. Symptomatic leaves were collected from various regions in Spain and Italy and mycelia associated to leaf lesions was harvested. Total RNA extractions were depleted of rRNA and metatranscriptomes were generated using a High-Throughput Sequencing approach. The virome associated to leaf lesions was then characterized through a bioinformatic pipeline relying on blast searches against current viral databases. Here we present an inventory of 283 new RNA viruses: 222 positive strand RNA viruses, 29 negative strand RNA viruses, 27 double stranded RNA viruses and 5 ORFan virus RdRP segments, which could not be reliably assigned to any existing group in the Riboviria. In addition to ORFan viruses, we found other surprising new evolutionary trajectories in this wide inventory of viruses. The most represented viruses in our collection are those in phylum Lenarviricota, and, among them, a group of mycovirus segments distantly related to narnaviruses, but characterized by a polymerase palm domain lacking subdomain C, with the putative GDD catalytic triad. We also provided evidence of a strict association between two RNA segments that form a new mycovirus clade of positive strand RNA in the phylum Kitrinoviricota, order Martellivirales. In the phylum Negarnaviricota, we report for the first time in the order Mononegavirales a clade of viruses that is ambisense, a feature that so far was present only in the order Bunyavirales. Furthermore, in the same phylum we detected the widespread occurrence and abundant accumulation in our libraries of a distinct mycovirus clade distantly related to the Muvirales and Goujanvirales orders, which so far include only viruses infecting invertebrates. Possible new oomycetes-specific virus clades are also described in the phylum Duplornaviricota. These data greatly expand the evolutionary history of mycoviruses adding new layers of diversity to the realm Riboviria.

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“…Interestingly, not all narnaviruses have an ambigrammatic genome (indeed, the example of Figure 1A is also in the Narnaviridae family). In agreement with previously reported observations 17 , overlaying the lengths of detectable rORFs on the narnavirus phylogeny shows that ambigrammatic sequences are present in at least two different clades. This finding, illustrated in Figure 3, indicates that the ambigrammatic feature is polyphyletic and may have been gained and lost multiple times in the evolution of this viral family.…”

Section: Introductionsupporting

confidence: 92%

“…Ambigrammatic narnavirus sequences have been identified in fungi 17 , where the mitochondrial genetic code uses only two stop codons. The fact that the narnavirus rORF sequences lack all three possible stop codons suggests that translation of the narnavirus rORF in these hosts is not occurring in the mitochondria, unlike viruses of the related Mitovirus genus 1 .…”

Section: Synonym Sudokumentioning

confidence: 99%

“…In contrast, Figure 1B shows the genetic sequence of Culex narnavirus 1, where one of the reverse reading frames also has an uninterrupted ORF spanning nearly the whole sequence. All known examples of ambigrammatic narnaviruses have the large reverse ORF in a reading frame where the codons are aligned with those in the forward direction 17 (i.e., in "frame −0" in the conventions of Figure 2). Figure 1C considers an intriguing intermediate case, which will be discussed further below.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

An exploration of ambigrammatic sequences in narnaviruses

DeRisi

Huber

Kistler

et al. 2019

Preprint

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Narnaviruses have been described as positive-sense RNA viruses with a remarkably 10 simple genome of ∼ 3 kb, encoding only a highly conserved RNA-dependent RNA polymerase 11 (RdRp). Many narnaviruses, however, are 'ambigrammatic' and harbor an additional uninterrupted 12 open reading frame (ORF) covering almost the entire length of the reverse complement strand. No 13 function has been described for this ORF, yet the absence of stops is conserved across diverse 14 narnaviruses, and in every case the codons in the reverse ORF and the RdRp are aligned. The > 3 kb 15 ORF overlap on opposite strands, unprecedented among RNA viruses, motivates an exploration of 16 the constraints imposed or alleviated by the codon alignment. Here, we show that only when the 17 codon frames are aligned can all stop codons be eliminated from the reverse strand by 18 synonymous single-nucleotide substitutions in the RdRp gene, suggesting a mechanism for de novo 19 gene creation within a strongly conserved amino-acid sequence. It will be fascinating to explore 20 what implications this coding strategy has for other aspects of narnavirus biology. Beyond 21 narnaviruses, our rapidly expanding catalog of viral diversity may yet reveal additional examples of 22 this broadly-extensible principle for ambigrammatic-sequence development. 23 24 42 235 MW thanks the Chan Zuckerberg Biohub for its hospitality. Author contributions: MW, DY and GH 236 7 of 13 Manuscript submitted to eLife conceived of the proposal and performed reading frame analysis. HR analyzed sequencing data 237 that stimulated this investigation, and generated the figures. JLD and AK provided critical input on 238 viral biology. HR, MW and DY wrote the manuscript with input from all authors.

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A case for a reverse-frame coding sequence in a group of positive-sense RNA viruses

Cited by 33 publications

References 72 publications

Metatranscriptomic Identification of Diverse and Divergent RNA Viruses in Green and Chlorarachniophyte Algae Cultures

Metatranscriptomic Identification of Diverse and Divergent RNA Viruses in Green and Chlorarachniophyte Algae Cultures

Analysis of the virome associated to grapevine downy mildew lesions reveals new mycovirus lineages

An exploration of ambigrammatic sequences in narnaviruses

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