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A second capsidless hadakavirus strain with 10 positive-sense single-stranded RNA genomic segments from Fusarium nygamai

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Abstract

A unique capsidless virus with a positive-sense, single-stranded RNA genome (hadakavirus 1, HadV1), a member of the extended picorna-like supergroup, was isolated previously from the phytopathogenic fungus Fusarium oxysporum. Here, we describe the molecular and biological characterisation of a second hadakavirus strain from Fusarium nygamai, which has not been investigated in detail previously as a virus host. This virus, hadakavirus 1 strain 1NL (HadV1-1NL), has features similar to the first hadakavirus, HadV1-7n, despite having a different number of segments (10 for HadV1-1NL vs. 11 for HadV1-7n). The 10 genomic RNA segments of HadV1-1NL range in size from 0.9 kb to 2.5 kb. All HadV1-1NL segments show 67% to 86% local nucleotide sequence identity to their HadV1-7n counterparts, whereas HadV1-1NL has no homolog of HadV1-7n RNA8, which encodes a zinc-finger motif. Another interesting feature is the possible coding incapability of HadV1-1NL RNA10. HadV1-1NL was predicted to be capsidless based on the RNase A susceptibility of its replicative form dsRNA. Phenotypic comparison of multiple virus-infected and virus-free single-spore isolates indicated asymptomatic infection by HadV1-1NL. Less-efficient vertical transmission via spores was observed as the infected fungal colonies from which the spores were derived became older, as was observed for HadV1-7n. This study shows a second example of a hadakavirus that appears to have unusual features.

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References

  1. Alastruey-Izquierdo A, Cuenca-Estrella M, Monzon A, Mellado E, Rodriguez-Tudela JL (2008) Antifungal susceptibility profile of clinical Fusarium spp. isolates identified by molecular methods. J Antimicrob Chemother 61:805–809

    Article  CAS  PubMed  Google Scholar 

  2. Appel DJ, Gordon TR (1996) Relationships among pathogenic and nonpathogenic isolates of Fusarium oxysporum based on the partial sequence of the intergenic spacer region of the ribosomal DNA. Mol Plant-Microbe Interact MPMI 9:125–138

    Article  CAS  PubMed  Google Scholar 

  3. Bormann J, Heinze C, Blum C, Mentges M, Brockmann A, Alder A, Landt SK, Josephson B, Indenbirken D, Spohn M, Plitzko B, Loesgen S, Freitag M, Schafer W (2018) Expression of a structural protein of the mycovirus FgV-ch9 negatively affects the transcript level of a novel symptom alleviation factor and causes virus-infection like symptoms in Fusarium graminearum. J Virol 92:e00326-e1318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Chiapello M, Rodriguez-Romero J, Ayllon MA, Turina M (2020) Analysis of the virome associated to grapevine downy mildew lesions reveals new mycovirus lineages. Virus Evol 6:veaa058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Chiba Y, Oiki S, Yaguchi T, Urayama SI, Hagiwara D (2021) Discovery of divided RdRp sequences and a hitherto unknown genomic complexity in fungal viruses. Virus Evol 7:veaa101

    Article  PubMed  Google Scholar 

  6. Cho WK, Lee KM, Yu J, Son M, Kim KH (2013) Insight into mycoviruses infecting Fusarium species. Adv Virus Res 86:273–288

    Article  CAS  PubMed  Google Scholar 

  7. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

    Article  PubMed  PubMed Central  Google Scholar 

  8. Donnell K, Kistler HC, Tacke BK, Casper HH (2000) Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum the fungus causing wheat scab. Proc Natl Acad Sci 97:7905

    Article  Google Scholar 

  9. Eusebio-Cope A, Suzuki N (2015) Mycoreovirus genome rearrangements associated with RNA silencing deficiency. Nucleic Acids Res 43:3802–3813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Heun Hong J, Gross KC (1998) Surface sterilization of whole tomato fruit with sodium hypochlorite influences subsequent postharvest behavior of fresh-cut slices. Postharvest Biol Technol 13:51–58

    Article  CAS  Google Scholar 

  11. Hillman BI, Fulbright DW, Nuss DL, Van Alfen NK (1995) Family Hypoviridae. In: Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD (eds) Virus taxonomy: sixth report of the international committee on taxonomy of viruses. Springer, New York, pp 261–264

    Google Scholar 

  12. Hisano S, Zhang R, Faruk MI, Kondo H, Suzuki N (2018) A neo-virus lifestyle exhibited by a (+)ssRNA virus hosted in an unrelated dsRNA virus: taxonomic and evolutionary considerations. Virus Res 244:75–83

    Article  CAS  PubMed  Google Scholar 

  13. Jamal A, Sato Y, Shahi S, Shamsi W, Kondo H, Suzuki N (2019) Novel victorivirus from a Pakistani isolate of Alternaria alternata lacking a typical translational stop/restart sequence signature. Viruses 11:577

    Article  CAS  PubMed Central  Google Scholar 

  14. Jia H, Dong K, Zhou L, Wang G, Hong N, Jiang D, Xu W (2017) A dsRNA virus with filamentous viral particles. Nat Commun 8:168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Kanhayuwa L, Kotta-Loizou I, Ozkan S, Gunning AP, Coutts RH (2015) A novel mycovirus from Aspergillus fumigatus contains four unique dsRNAs as its genome and is infectious as dsRNA. Proc Natl Acad Sci USA 112:9100–9105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166

    Article  CAS  PubMed  Google Scholar 

  17. Koonin EV, Wolf YI, Nagasaki K, Dolja VV (2008) The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat Rev Microbiol 6:925–939

    Article  CAS  PubMed  Google Scholar 

  18. Koonin EV, Dolja VV (2014) Virus world as an evolutionary network of viruses and capsidless selfish elements. Microbiol Mol Biol Rev 78:278–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI, Yutin N, Zerbini FM, Kuhn JH (2020) Global organization and proposed megataxonomy of the virus world. Microbiol Mol Biol Rev 84:e00061-e119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kotta-Loizou I, Coutts RHA (2017) Studies on the virome of the entomopathogenic fungus Beauveria bassiana reveal novel dsRNA elements and mild hypervirulence. PLoS Pathog 13:e1006183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Kotta-Loizou I, Caston JR, Coutts RHA, Hillman BI, Jiang D, Kim DH, Moriyama H, Suzuki N, ICTV Report C (2020) ICTV virus taxonomy profile: Chrysoviridae. J Gen Virol 99:19–20

    Google Scholar 

  22. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Li P, Bhattacharjee P, Wang S, Zhang L, Ahmed I, Guo L (2019) Mycoviruses in Fusarium species: an update. Front Cell Infect Microbiol 9:257. https://doi.org/10.3389/fcimb.2019.00257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li PF, Wang SC, Zhang LH, Qiu DW, Zhou XP, Guo LH (2020) A tripartite ssDNA mycovirus from a plant pathogenic fungus is infectious as cloned DNA and purified virions. Sci Adv 6:eaay9634. https://doi.org/10.1126/sciadv.aay9634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Mizutani Y, Abraham A, Uesaka K, Kondo H, Suga H, Suzuki N, Chiba S (2018) Novel mitoviruses and a unique tymo-like virus in hypovirulent and virulent strains of the Fusarium head bight fungus, Fusarium boothii. Viruses 10:E584

    Article  PubMed  CAS  Google Scholar 

  26. Nalim FA, Elmer WH, McGovern RJ, Geiser DM (2009) Multilocus phylogenetic diversity of Fusarium avenaceum pathogenic on lisianthus. Phytopathology 99:462–468

    Article  CAS  PubMed  Google Scholar 

  27. Nerva L, Forgia M, Ciuffo M, Chitarra W, Chiapello M, Vallino M, Varese GC, Turina M (2019) The mycovirome of a fungal collection from the sea cucumber Holothuria polii. Virus Res 273:197737

    Article  CAS  PubMed  Google Scholar 

  28. O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465–493

    Article  CAS  Google Scholar 

  29. O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci 95:2044

    Article  PubMed  PubMed Central  Google Scholar 

  30. O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, Riley R, Zitomer NC, Colyer P, Waalwijk C, Tvd L, Moretti A, Kang S, Kim H-S, Geiser DM, Juba JH, Baayen RP, Cromey MG, Bithell S, Sutton DA, Skovgaard K, Ploetz R, Corby Kistler H, Elliott M, Davis M, Sarver BAJ (2009) A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genet Biol 46:936–948

    Article  PubMed  CAS  Google Scholar 

  31. Sato Y, Jamal A, Kondo H, Suzuki N (2020) Molecular characterization of a novel polymycovirus from Penicillium janthinellum with a focus on its genome-associated PASrp. Front Microbiol 11:592789

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sato Y, Shamsi W, Jamal A, Bhatti MF, Kondo H, Suzuki N (2020) Hadaka virus 1: a capsidless eleven-segmented positive-sense single-stranded RNA virus from a phytopathogenic fungus, Fusarium oxysporum. MBio 11:e00450-20.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Shamsi W, Sato Y, Jamal A, Shahi S, Kondo H, Suzuki N, Bhatti MF (2019) Molecular and biological characterization of a novel botybirnavirus identified from a Pakistani isolate of Alternaria alternata. Virus Res 263:119–128

    Article  CAS  PubMed  Google Scholar 

  34. Son M, Lee KM, Yu J, Kang M, Park JM, Kwon SJ, Kim KH (2013) The HEX1 gene of Fusarium graminearum is required for fungal asexual reproduction and pathogenesis and for efficient viral RNA accumulation of Fusarium graminearum virus 1. J Virol 87:10356–10367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Sun L, Suzuki N (2008) Intragenic rearrangements of a mycoreovirus induced by the multifunctional protein p29 encoded by the prototypic hypovirus CHV1-EP713. RNA 14:2557–2571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Sutela S, Forgia M, Vainio EJ, Chiapello M, Daghino S, Vallino M, Martino E, Girlanda M, Perotto S, Turina M (2020) The virome from a collection of endomycorrhizal fungi reveals new viral taxa with unprecedented genome organization. Virus Evol 6:veaa076

    Article  PubMed  PubMed Central  Google Scholar 

  37. Suzuki N, Watanabe Y, Kusano T, Kitagawa Y (1990) Sequence analysis of rice dwarf phytoreovirus genome segments S4, S5, and S6: comparison with the equivalent wound tumor virus segments. Virology 179:446–454

    Article  CAS  PubMed  Google Scholar 

  38. Suzuki N, Maruyama K, Moriyama M, Nuss DL (2003) Hypovirus papain-like protease p29 functions in trans to enhance viral double-stranded RNA accumulation and vertical transmission. J Virol 77:11697–11707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Suzuki N, Supyani S, Maruyama K, Hillman BI (2004) Complete genome sequence of Mycoreovirus-1/Cp9B21, a member of a novel genus within the family Reoviridae, isolated from the chestnut blight fungus Cryphonectria parasitica. J Gen Virol 85:3437–3448

    Article  CAS  PubMed  Google Scholar 

  40. Suzuki N, Ghabrial SA, Kim KH, Pearson M, Marzano SL, Yaegashi H, Xie J, Guo L, Kondo H, Koloniuk I, Hillman BI, ICTV Report C (2018) ICTV virus taxonomy profile: Hypoviridae. J Gen Virol 99:615–616

    Article  CAS  PubMed  Google Scholar 

  41. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577

    Article  CAS  PubMed  Google Scholar 

  42. Urayama S, Katoh Y, Fukuhara T, Arie T, Moriyama H, Teraoka T (2015) Rapid detection of Magnaporthe oryzae chrysovirus 1-A from fungal colonies on agar plates and lesions of rice blast. J Gen Plant Pathol 81:97–102

    Article  Google Scholar 

  43. Valverde RA, Khalifa ME, Okada R, Fukuhara T, Sabanadzovic S, Ictv Report C (2019) ICTV virus taxonomy profile: Endornaviridae. J Gen Virol 100:1204–1205

    Article  CAS  PubMed  Google Scholar 

  44. Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM, Dempsey DM, Dutilh BE, Harrach B, Harrison RL, Hendrickson RC, Junglen S, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Nibert M, Orton RJ, Rubino L, Sabanadzovic S, Simmonds P, Smith DB, Varsani A, Zerbini FM, Davison AJ (2020) Changes to virus taxonomy and the statutes ratified by the International Committee on Taxonomy of Viruses (2020). Arch Virol 165:2737–2748

    Article  CAS  PubMed  Google Scholar 

  45. Wei CZ, Osaki H, Iwanami T, Matsumoto N, Ohtsu Y (2004) Complete nucleotide sequences of genome segments 1 and 3 of Rosellinia anti-rot virus in the family Reoviridae. Arch Virol 149:773–777

    Article  CAS  PubMed  Google Scholar 

  46. White T, Bruns T, Lee S, Taylor J, Innis M, Gelfand D, Sninsky J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc Guide Methods Appl. 18:315–322

    Google Scholar 

  47. Wickner RB, Fujimura T, Esteban R (2013) Viruses and prions of Saccharomyces cerevisiae. Adv Virus Res 86:1–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Wolf YI, Kazlauskas D, Iranzo J, Lucia-Sanz A, Kuhn JH, Krupovic M, Dolja VV, Koonin EV (2018) Origins and evolution of the global RNA virome. MBio 9: e02329-18

    Article  PubMed  PubMed Central  Google Scholar 

  49. Yu J, Lee KM, Cho WK, Park JY, Kim KH (2018) Differential contribution of RNA interference components in response to distinct Fusarium graminearum virus infections. J Virol 92:e01756-01717

    Article  Google Scholar 

  50. Zhai L, Xiang J, Zhang M, Fu M, Yang Z, Hong N, Wang G (2016) Characterization of a novel double-stranded RNA mycovirus conferring hypovirulence from the phytopathogenic fungus Botryosphaeria dothidea. Virology 493:75–85

    Article  CAS  PubMed  Google Scholar 

  51. Zhang R, Hisano S, Tani A, Kondo H, Kanematsu S, Suzuki N (2016) A capsidless ssRNA virus hosted by an unrelated dsRNA virus. Nat Microbiol 1:15001.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to Dr. Sabitree Shahi and Ms. Sakae Hisano for technical assistance. HAK is thankful to the Higher Education Commission (HEC) of Pakistan for a fellowship under the International Research Support Initiative Program (IRSIP). YS is a JSPS (Japan Society for the Promotion of Science) fellow.

Funding

This study was supported in part by Yomogi Inc., the Ohara Foundation for Agriculture Research (to NS), Grants-in-Aid for Scientific Research on Innovative Areas from the Japanese Ministry of Education, Culture, Sports, Science and Technology (KAKENHI 17H01463, 16H06436, 16H06429 and 16K21723 to N.S. and H.K.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Contributions

Conceptualization, NS; investigation, HAK, YS, AJ, HK, and NS; supervision, AJ and MFB; writing—original draft, HAK, YS, and NS; writing—reviewing and editing, AJ, MFB, and HK; funding acquisition, NS.

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Correspondence to Muhammad Faraz Bhatti or Nobuhiro Suzuki.

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The authors declare that there are no conflicts of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

Sequence data availability

The complete genomic nucleotide sequence of HadV1-1NL was deposited in the GenBank/ENA/DDBJ database under accession numbers LC592214 to LC592223.

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Handling Editor: Ioly Kotta-Loizou.

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Khan, H.A., Sato, Y., Kondo, H. et al. A second capsidless hadakavirus strain with 10 positive-sense single-stranded RNA genomic segments from Fusarium nygamai. Arch Virol 166, 2711–2722 (2021). https://doi.org/10.1007/s00705-021-05176-x

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