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Cited by 34Bacteriophages and microbial interactionsPlant and Fungal Interactions ResearchMicrobial Community Ecology and Physiology

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Double-stranded RNA sequencing reveals distinct riboviruses associated with thermoacidophilic bacteria from hot springs in Japan

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Urayama, Syun-ichi, Fukudome, Akihito, Hirai, Miho, Okumura, Tomoyo, Nishimura, Yosuke, Takaki, Yoshihiro, Kurosawa, Norio, Koonin, Eugene V., Krupovic, Mart, Nunoura, Takuro·2024·Nature Microbiology
DOI 10.1038/s41564-023-01579-5PMC PMC10847044

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Abstract

Metatranscriptome sequencing expanded the known diversity of the bacterial RNA virome, suggesting that additional riboviruses infecting bacterial hosts remain to be discovered. Here we employed double-stranded RNA sequencing to recover complete genome sequences of two ribovirus groups from acidic hot springs in Japan. One group, denoted hot spring riboviruses (HsRV), consists of viruses with distinct RNA-directed RNA polymerases (RdRPs) that seem to be intermediates between typical ribovirus RdRPs and viral reverse transcriptases. This group forms a distinct phylum, Artimaviricota , or even kingdom within the realm Riboviria . We identified viruses encoding HsRV-like RdRPs in marine water, river sediments and salt marshes, indicating that this group is widespread beyond extreme ecosystems. The second group, denoted hot spring partiti-like viruses (HsPV), forms a distinct branch within the family Partitiviridae . The genome architectures of HsRV and HsPV and their identification in bacteria-dominated habitats suggest that these viruses infect thermoacidophilic bacteria.

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Research works printed but not linked: 43

  1. Simmonds, P. et al. Consensus statement: virus taxonomy in the age of metagenomics. Nat. Rev. Microbiol. 15, 161–168 (2017). · DOI
  2. Shi, M. et al. Redefining the invertebrate RNA virosphere. Nature 540, 539–543 (2016). · DOI
  3. Wolf, Y. I. et al. Origins and evolution of the global RNA virome. mBio 9, e02329-18 (2018). · DOI
  4. Wolf, Y. I. et al. Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome. Nat. Microbiol. 5, 1262–1270 (2020). · DOI
  5. Shi, M., Zhang, Y. Z. & Holmes, E. C. Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Res. 243, 83–90 (2018). · DOI
  6. Shi, M. et al. The evolutionary history of vertebrate RNA viruses. Nature 556, 197–202 (2018). · DOI
  7. Zayed, A. A. et al. Cryptic and abundant marine viruses at the evolutionary origins of Earth’s RNA virome. Science 376, 156–162 (2022). · DOI
  8. Neri, U. et al. Expansion of the global RNA virome reveals diverse clades of bacteriophages. Cell 185, 4023–4037 (2022). · DOI
  9. Edgar, R. C. et al. Petabase-scale sequence alignment catalyses viral discovery. Nature 602, 142–147 (2022). · DOI
  10. Koonin, E. V. et al. Global organization and proposed megataxonomy of the virus world. Microbiol. Mol. Biol. Rev. 84, e00061-19 (2020). · DOI
  11. Koonin, E. V., Dolja, V. V. & Krupovic, M. Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479-480, 2–25 (2015). · DOI
  12. Nasir, A., Forterre, P., Kim, K. M. & Caetano-Anolles, G. The distribution and impact of viral lineages in domains of life. Front. Microbiol. 5, 194 (2014). · DOI
  13. Callanan, J. et al. Leviviricetes: expanding and restructuring the taxonomy of bacteria-infecting single-stranded RNA viruses. Microb. Genomics 7, 000686 (2021). · DOI
  14. Callanan, J. et al. Expansion of known ssRNA phage genomes: from tens to over a thousand. Sci. Adv. 6, eaay5981 (2020). · DOI
  15. Krishnamurthy, S. R., Janowski, A. B., Zhao, G., Barouch, D. & Wang, D. Hyperexpansion of RNA bacteriophage diversity. PLoS Biol. 14, e1002409 (2016). · DOI
  16. Morris, T. J. & Dodds, J. A. Isolation and analysis of double-stranded-RNA from virus-infected plant and fungal tissue. Phytopathology 69, 854–858 (1979).
  17. Hirai, M. et al. RNA viral metagenome analysis of subnanogram dsRNA using fragmented and primer ligated dsRNA sequencing (FLDS). Microbes Environ. 36, ME20152 (2021). · DOI
  18. Urayama, S., Takaki, Y. & Nunoura, T. FLDS: a comprehensive dsRNA sequencing method for intracellular RNA virus surveillance. Microbes Environ. 31, 33–40 (2016). · DOI
  19. Urayama, S. et al. Unveiling the RNA virosphere associated with marine microorganisms. Mol. Ecol. Resour. 18, 1444–1455 (2018). · DOI
  20. Gruber-Vodicka, H. R., Seah, B. K. & Pruesse, E. phyloFlash: rapid small-subunit rRNA profiling and targeted assembly from metagenomes. mSystems 5, e00920 (2020). · DOI
  21. Yang, Y. et al. Characterization of the first double-stranded RNA bacteriophage infecting Pseudomonas aeruginosa. Sci. Rep. 6, 38795 (2016). · DOI
  22. Venkataraman, S., Prasad, B. & Selvarajan, R. RNA dependent RNA polymerases: insights from structure, function and evolution. Viruses 10, 76 (2018). · DOI
  23. Te Velthuis, A. J. Common and unique features of viral RNA-dependent polymerases. Cell. Mol. Life Sci. 71, 4403–4420 (2014). · DOI
  24. Forgia, M. et al. Hybrids of RNA viruses and viroid-like elements replicate in fungi. Nat. Commun. 14, 2591 (2023). · DOI
  25. Krupovic, M. et al. Ortervirales: new virus order unifying five families of reverse-transcribing viruses. J. Virol. 92, e00515–18 (2018). · DOI
  26. Luque, D., Mata, C. P., Suzuki, N., Ghabrial, S. A. & Castón, J. R. Capsid structure of dsRNA fungal viruses. Viruses 10, 481 (2018). · DOI
  27. Byrne, M., Kashyap, A., Esquirol, L., Ranson, N. & Sainsbury, F. The structure of a plant-specific partitivirus capsid reveals a unique coat protein domain architecture with an intrinsically disordered protrusion. Commun. Biol. 4, 1155 (2021). · DOI
  28. Duquerroy, S. et al. The picobirnavirus crystal structure provides functional insights into virion assembly and cell entry. EMBO J. 28, 1655–1665 (2009). · DOI
  29. Krishnamurthy, S. R. & Wang, D. Extensive conservation of prokaryotic ribosomal binding sites in known and novel picobirnaviruses. Virology 516, 108–114 (2018). · DOI · Paper page
  30. Peyambari, M., Guan, S. & Roossinck, M. J. RdRp or RT, that is the question. Mol. Biol. Evol. 38, 5082–5091 (2021). · DOI
  31. Okada, R., Kiyota, E., Moriyama, H., Fukuhara, T. & Natsuaki, T. A simple and rapid method to purify viral dsRNA from plant and fungal tissue. J. Gen. Plant Pathol. 81, 103–107 (2015). · DOI
  32. Urayama, S., Takaki, Y., Hagiwara, D. & Nunoura, T. dsRNA-seq reveals novel RNA virus and virus-like putative complete genome sequences from Hymeniacidon sp. sponge. Microbes Environ. 35, ME19132 (2020). · DOI
  33. Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010). · DOI
  34. Gabler, F. et al. Protein sequence analysis using the MPI bioinformatics toolkit. Curr. Protoc. Bioinformatics 72, e108 (2020). · DOI · Paper page
  35. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013). · DOI
  36. Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567–580 (2001). · DOI · Paper page
  37. Camargo, A. P. et al. IMG/VR v4: an expanded database of uncultivated virus genomes within a framework of extensive functional, taxonomic, and ecological metadata. Nucleic Acids Res. 51, D733–D743 (2023). · DOI · Paper page
  38. Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021). · DOI
  39. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013). · DOI · Paper page
  40. Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009). · DOI
  41. Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020). · DOI · Paper page
  42. Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017). · DOI · Paper page
  43. Pei, J. & Grishin, N. V. PROMALS3D: multiple protein sequence alignment enhanced with evolutionary and three-dimensional structural information. Methods Mol. Biol. 1079, 263–271 (2014). · DOI

Metadata

Authors
Urayama, S.-I., Fukudome, A., Hirai, M., Okumura, T., Nishimura, Y., Takaki, Y., Kurosawa, N., Koonin, E. V., Krupovic, M., & Nunoura, T.
Affiliations
  • University of Tsukuba (JP)
  • Howard Hughes Medical Institute (US)
  • Japan Agency for Marine-Earth Science and Technology (JP)
  • Marine Core Research Institute, Kochi University (JP)
  • Soka University (JP)
  • National Institutes of Health (US)
Corresponding author
Urayama, Syun-ichi
ORCID
Venue
Nature Microbiology
Publisher
Springer Science and Business Media LLC
Published
2024-01-17
Volume
9
Issue
2
Pages
514-523
ISSN
2058-5276 (ISSN-L)
DOI
10.1038/s41564-023-01579-5
PMC
PMC10847044
OpenAlex
W4390947644
Cited by
34
References
3
Citations by year
2026: 8 · 2025: 11 · 2024: 15
FWCI
9.30
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Microbiology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
  • HAL (submittedVersion, cc-by)
  • Institutional Repositories DataBase (IRDB) (submittedVersion)
  • Terrestrial Environment Research Center (University of Tsukuba) (submittedVersion, cc-by)
Funders
  • JSPS | Japan Society for the Promotion of Science
  • MEXT | Japan Society for the Promotion of Science (19H05684, 16H06429, 16K21723, 16H06437)
Topics
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Immunology and Microbiology › Virology › Plant and Fungal Interactions Research
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
thermoacidophilic bacteria, hot springs, double-stranded RNA virus, RNA-dependent RNA polymerase, Partitiviridae, viral evolution, metatranscriptomics

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