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A capsidless ssRNA virus hosted by an unrelated dsRNA virus

Nature Microbiology volume 1, Article number: 15001 (2016) Cite this article

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Abstract

Viruses typically encode the capsid that encases their genome, while satellite viruses do not encode a replicase and depend on a helper virus for their replication1. Here, we report interplay between two RNA viruses, yado-nushi virus 1 (YnV1) and yado-kari virus 1 (YkV1), in a phytopathogenic fungus, Rosellinia necatrix2. YkV1 has a close phylogenetic affinity to positive-sense, single-stranded (+)ssRNA viruses such as animal caliciviruses3, while YnV1 has an undivided double-stranded (ds) RNA genome with a resemblance to fungal totiviruses4. Virion transfection and infectious full-length cDNA transformation has shown that YkV1 depends on YnV1 for viability, although it probably encodes functional RNA-dependent RNA polymerase (RdRp). Immunological and molecular analyses have revealed trans-encapsidation of not only YkV1 RNA but also RdRp by the capsid protein of the other virus (YnV1), and enhancement of YnV1 accumulation by YkV1. This study demonstrates interplay in which the capsidless (+)ssRNA virus (YkV1), hijacks the capsid protein of the dsRNA virus (YnV1), and replicates as if it were a dsRNA virus.

Lower eukaryotes, including fungi, amoebae and algae, are important as virus hosts, and a rapidly growing number of viruses have been reported from these in the past few decades5–8. These have contributed to further enhance our understanding of virus evolution and diversity. At the same time, some unusual viruses have shown their peculiarity and challenged the ‘common rules’ of viruses in terms of size and concept. One such virus group includes the so-called double-stranded (ds) DNA megaviruses (mimiviruses, pandoraviruses)9. Viruses were classically defined as nano-organisms (infectious virions with capsids encasing their genomes) that can pass through a bacteria-proof filter candle. However, the giant DNA viruses exceed bacterial parasites such as mycoplasmas in their genome (>1.2 Mb) and particle size (>0.5 μm)10. Other unusual examples include ‘naked’ or ‘capsidless’ viruses, exemplified by the fungal hypoviruses11. In addition, several groups of capsidless viruses such as umbraviruses, endornaviruses and narnaviruses are now recognized that infect either plants or fungi3,12,13. These capsidless viruses are considered to be positive-sense (+) single-stranded (ss) RNA viruses based on their phylogeny, using hallmark proteins such as RNA-dependent RNA polymerase (RdRp). Capsidless narnaviruses with genomes of ∼2.3–3.6 kb represent a minimal virus form14, encoding only RdRp, while others have relatively complex genome architectures.

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Figure 1: Characterization of yado-nushi virus 1 (YnV1) and yado-kari virus 1 (YkV1) infecting R. necatrix strain W1032 and composition of virus particles isolated from it.
Figure 2: Interaction between YnV1 and YkV1.
Figure 3: Proposed model for interactions between YnV1 and YkV1.

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Acknowledgements

The authors acknowledge Yomogi Inc. (N.S.) and the Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries and food Industry (25032AB) (S.K. and N.S.) for financial support during this study. The authors thank R. Dietzgen, K. Hyodo and I.B. Andika for discussions and critical reading of the manuscript. The authors are also grateful to T. Shiokawa and H. Tada at the Division of Instrumental Analysis, Okayama University, for the amino-acid sequence analyses.

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Author notes

  1. Rui Zhang and Sakae Hisano: These authors contributed equally to this work.

Authors and Affiliations

  1. Agrivirology Laboratory, Institute of Plant Science and Resources, Okayama University, Chuou 2-20-1, Kurashiki, 710-0046, Okayama, Japan

    Rui Zhang, Sakae Hisano, Akio Tani, Hideki Kondo & Nobuhiro Suzuki

  2. NARO Institute of Fruit Tree Science, 92 Shimokuriyagawa, Morioka, 020-0123, Iwate, Japan

    Satoko Kanematsu

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  1. Rui Zhang
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Contributions

S.K. and N.S. designed the research. R.Z., S.H., A.T. and H.K. performed the experiments. S.K. contributed fungal materials. H.K., A.T. and N.S. analysed the data. N.S. wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Nobuhiro Suzuki.

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Zhang, R., Hisano, S., Tani, A. et al. A capsidless ssRNA virus hosted by an unrelated dsRNA virus. Nat Microbiol 1, 15001 (2016). https://doi.org/10.1038/nmicrobiol.2015.1

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