1887

Journal of General Virology header logo

Volume 104, Issue 11

Molecular and biological characterization of a partitivirus from Open Access

Abstract

is a thermo-tolerant, ubiquitous fungus commonly found in food products, indoor environments, soil and clinical samples. It is a well-known biocontrol agent used against phytopathogenic fungi and its metabolites have many industrial applications. Rare reports of related human infections have been found in the medical literature. In this study, we report for the first time the infection of isolated from a soil sample collected in a rice field with a double-stranded RNA virus, Paeciliomyces variotii partitivirus 1 (PvPV-1) in the family harboured icosahedral virus particles 30 nm in diameter with two dsRNA segments 1758 and 1356 bp long. Both dsRNA1 and dsRNA2 have a single open reading frame encoding proteins of 63 and 40 kDa, respectively. These proteins have significant similarity to the RNA-dependent RNA polymerase and capsid protein encoded by the genomic segments of several viruses from the family . Phylogenetic analysis revealed that PvPV-1 belongs to the family but in an unclassified group/genus, tentatively nominated Zetapartitivirus. PvPV-1 was found to increase the growth rate of the host fungus, as indicated by time course experiments performed on a range of different media for virus-infected and virus-free isogenic lines. Further, dual-culture assays performed for both isogenic lines confirmed the antagonistic potential of against other phytopathogenic fungi. The findings of this study assist us in understanding as a potential biocontrol agent, together with plant–fungus–virus interactions.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): biological control , double-stranded RNA , growth , metabolism , Paecilomyces variotii , Partitiviridae and zetapartitivirus
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001925
2023-11-28
2024-09-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/104/11/jgv001925.html?itemId=/content/journal/jgv/10.1099/jgv.0.001925&mimeType=html&fmt=ahah

References

  1. El Komy MH, Saleh AA, Eranthodi A, Molan YY. Characterization of novel Trichoderma asperellum isolates to select effective biocontrol agents against tomato fusarium wilt. Plant Pathol J 2015; 31:50–60 [View Article] [PubMed]
     [Google Scholar]
  2. Treseder KK, Lennon JT. Fungal traits that drive ecosystem dynamics on land. Microbiol Mol Biol Rev 2015; 79:243–262 [View Article] [PubMed]
     [Google Scholar]
  3. Jayne B, Quigley M. Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis. Mycorrhiza 2014; 24:109–119 [View Article] [PubMed]
     [Google Scholar]
  4. Ramachandra TV, Bharath S, Gupta N. Modelling landscape dynamics with LST in protected areas of Western Ghats, Karnataka. J Environ Manage 2018; 206:1253–1262 [View Article] [PubMed]
     [Google Scholar]
  5. Hannula SE, Morriën E, de Hollander M, van der Putten WH, van Veen JA et al. Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture. ISME J 2017; 11:2294–2304 [View Article] [PubMed]
     [Google Scholar]
  6. Vainio EJ, Pennanen T, Rajala T, Hantula J. Occurrence of similar mycoviruses in pathogenic, saprotrophic and mycorrhizal fungi inhabiting the same forest stand. FEMS Microbiol Ecol 2017; 93: [View Article] [PubMed]
     [Google Scholar]
  7. Myers JM, Bonds AE, Clemons RA, Thapa NA, Simmons DR et al. Erratum for Myers et al., “survey of early-diverging lineages of fungi reveals abundant and diverse mycoviruses.”. mBio 2020; 11:e02027–20 [View Article] [PubMed]
     [Google Scholar]
  8. Gilbert KB, Holcomb EE, Allscheid RL, Carrington JC. Hiding in plain sight: new virus genomes discovered via a systematic analysis of fungal public transcriptomes. PLoS One 2019; 14:e0219207 [View Article] [PubMed]
     [Google Scholar]
  9. Li P, Wang S, Zhang L, Qiu D, Zhou X et al. A tripartite ssDNA mycovirus from a plant pathogenic fungus is infectious as cloned DNA and purified virions. Sci Adv 2020; 6:eaay9634 [View Article] [PubMed]
     [Google Scholar]
  10. Lin Y-H, Fujita M, Chiba S, Hyodo K, Andika IB et al. Two novel fungal negative-strand RNA viruses related to mymonaviruses and phenuiviruses in the shiitake mushroom (Lentinula edodes). Virology 2019; 533:125–136 [View Article] [PubMed]
     [Google Scholar]
  11. Liu L, Xie J, Cheng J, Fu Y, Li G et al. Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses. Proc Natl Acad Sci USA 2014; 111:12205–12210 [View Article] [PubMed]
     [Google Scholar]
  12. Ruiz-Padilla A, Rodríguez-Romero J, Gómez-Cid I, Pacifico D, Ayllón MA et al. Novel mycoviruses discovered in the mycovirome of a necrotrophic fungus. mBio 2021; 12:e03705–20 [View Article] [PubMed]
     [Google Scholar]
  13. Yu X, Li B, Fu Y, Jiang D, Ghabrial SA et al. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 2010; 107:8387–8392 [View Article] [PubMed]
     [Google Scholar]
  14. Ghabrial SA. Origin, adaptation and evolutionary pathways of fungal viruses. Virus genes 1998; 16:119–131 [View Article] [PubMed]
     [Google Scholar]
  15. Sutela S, Poimala A, Vainio EJ. Viruses of fungi and oomycetes in the soil environment. FEMS Microbiol Ecol 2019; 95: [View Article] [PubMed]
     [Google Scholar]
  16. Tiago PV, Fungaro MHP, de Faria MR, Furlaneto MC. Effects of double-stranded RNA in Metarhizium anisopliae VAR. acridum and Paecilomyces fumosoroseus on protease activities, conidia production, and virulence. Can J Microbiol 2004; 50:335–339 [View Article] [PubMed]
     [Google Scholar]
  17. Inglis PW, Valadares-Inglis MC. Rapid isolation of double-stranded RNAs from entomopathogenic species of the fungus Paecilomyces using a commercial minicolumn system. J Virol Methods 1997; 67:113–116 [View Article] [PubMed]
     [Google Scholar]
  18. Moreno-Gavíra A, Diánez F, Sánchez-Montesinos B, Santos M. Biocontrol effects of Paecilomyces variotii against fungal plant diseases. J Fungi 2021; 7:415 [View Article] [PubMed]
     [Google Scholar]
  19. Mioso R, Toledo Marante FJ, Herrera Bravo de Laguna I. The chemical diversity of the ascomycete fungus Paecilomyces variotii. Appl Biochem Biotechnol 2015; 177:781–791 [View Article] [PubMed]
     [Google Scholar]
  20. Kotta-Loizou I. Mycoviruses and their role in fungal pathogenesis. Curr Opin Microbiol 2021; 63:10–18 [View Article] [PubMed]
     [Google Scholar]
  21. Coenen A, Kevei F, Hoekstra RF. Factors affecting the spread of double-stranded RNA viruses in Aspergillus nidulans. Genet Res 1997; 69:1–10 [View Article] [PubMed]
     [Google Scholar]
  22. Hirai M, Takaki Y, Kondo F, Horie M, Urayama S et al. RNA viral metagenome analysis of subnanogram dsRNA using fragmented and primer ligated dsRNA sequencing (FLDS). Microb Environ 2021; 36:n [View Article] [PubMed]
     [Google Scholar]
  23. Vancov T, Keen B. Amplification of soil fungal community DNA using the ITS86F and ITS4 primers. FEMS Microbiol Lett 2009; 296:91–96 [View Article] [PubMed]
     [Google Scholar]
  24. White TJ, Bruns T, Lee S, Taylor J. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. PCR Protocols: A Guide to Methods and Applications 1990 pp 315–322
     [Google Scholar]
  25. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinformatics 2019; 20:1160–1166 [View Article] [PubMed]
     [Google Scholar]
  26. Tamura K, Stecher G, Kumar S, Battistuzzi FU. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
     [Google Scholar]
  27. Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL. The vienna RNA websuite. Nucleic Acids Res 2008; 36:W70–W74 [View Article] [PubMed]
     [Google Scholar]
  28. Jamal A, Sato Y, Shahi S, Shamsi W, Kondo H et al. Novel victorivirus from a Pakistani isolate of alternaria alternata lacking a typical translational stop/restart sequence signature. Viruses 2019; 11:577 [View Article] [PubMed]
     [Google Scholar]
  29. Shamsi W, Sato Y, Jamal A, Shahi S, Kondo H et al. Molecular and biological characterization of a novel botybirnavirus identified from a Pakistani isolate of Alternaria alternata. Virus Research 2019; 263:119–128 [View Article]
     [Google Scholar]
  30. Santos DA, Shi L, Tu BP, Weissman JS. Cycloheximide can distort measurements of mRNA levels and translation efficiency. Nucleic Acids Res 2019; 47:4974–4985 [View Article] [PubMed]
     [Google Scholar]
  31. Dalzoto PR, Glienke-Blanco C, Kava-Cordeiro V, Ribeiro JZ, Kitajima EW et al. Horizontal transfer and hypovirulence associated with double-stranded RNA in Beauveria bassiana. Mycol Res 2006; 110:1475–1481 [View Article] [PubMed]
     [Google Scholar]
  32. Jamal A. Incidence and characterisation of mycoviruses from Aspergillus fumigatus; 2010
  33. Scudiero DA, Shoemaker RH, Paull KD, Monks A, Tierney S et al. Evaluation of a soluble tetrazolium/Formazan assay for cell growth and drug sensitivity in culture using human and other tumor cell lines. Cancer Res 1988; 48:4827–4833
     [Google Scholar]
  34. Ferreira JAG, Penner JC, Moss RB, Haagensen JAJ, Clemons KV et al. Inhibition of Aspergillus fumigatus and its biofilm by Pseudomonas aeruginosa is dependent on the source, phenotype and growth conditions of the bacterium. PLoS One 2015; 10:e0134692 [View Article] [PubMed]
     [Google Scholar]
  35. Yassin MT, Mostafa A-F, Al-Askar AA, Sayed SRM, Rady AM. Antagonistic activity of Trichoderma harzianum and Trichoderma viride strains against some fusarial pathogens causing stalk rot disease of maize, in vitro. J King Saud University - Sci 2021; 33:101363 [View Article]
     [Google Scholar]
  36. Rahman MA, Begum MF, Alam MF. Screening of trichoderma isolates as a biological control agent against Ceratocystis paradoxa causing pineapple disease of sugarcane. Mycobiology 2009; 37:277–285 [View Article] [PubMed]
     [Google Scholar]
  37. Bruenn JA. A closely related group of RNA-dependent RNA polymerases from double-stranded RNA viruses. Nucleic Acids Res 1993; 21:5667–5669 [View Article] [PubMed]
     [Google Scholar]
  38. Jiang Y, Wang J, Yang B, Wang Q, Zhou J et al. Molecular characterization of a debilitation-associated partitivirus infecting the pathogenic fungus Aspergillus flavus. Front Microbiol 2019; 10:626 [View Article] [PubMed]
     [Google Scholar]
  39. Nibert ML, Ghabrial SA, Maiss E, Lesker T, Vainio EJ et al. Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Res 2014; 188:128–141 [View Article] [PubMed]
     [Google Scholar]
  40. Compel P, Papp I, Bibo´ M, Fekete C, Hornok L. Genetic interrelationships and genome organization of double-stranded RNA elements of Fusarium poae. Virus genes 1999; 18:49–56 [View Article]
     [Google Scholar]
  41. Thapa V, Keller NP, Roossinck MJ. Evaluation of virus-free and wild-type isolates of Pseudogymnoascus destructans using a porcine ear model. mSphere 2022; 7:e0102221 [View Article] [PubMed]
     [Google Scholar]
  42. Kim J-M, Song H-Y, Choi H-J, Yun S-H, So K-K et al. Changes in the mycovirus (LeV) titer and viral effect on the vegetative growth of the edible mushroom Lentinula edodes. Virus Res 2015; 197:8–12 [View Article] [PubMed]
     [Google Scholar]
  43. Song H-Y, Choi H-J, Jeong H, Choi D, Kim D-H et al. Viral effects of a dsRNA mycovirus (PoV-ASI2792) on the vegetative growth of the edible mushroom Pleurotus ostreatus. Mycobiology 2016; 44:283–290 [View Article] [PubMed]
     [Google Scholar]
  44. Singh U, Akhtar S, Mishra A, Sarkar D. A novel screening method based on menadione mediated rapid reduction of tetrazolium salt for testing of anti-mycobacterial agents. J Microbiol Methods 2011; 84:202–207 [View Article] [PubMed]
     [Google Scholar]
  45. Urquhart AS, Mondo SJ, Mäkelä MR, Hane JK, Wiebenga A et al. Genomic and genetic insights into a cosmopolitan fungus, Paecilomyces variotii (Eurotiales). Front Microbiol 2018; 9:3058 [View Article] [PubMed]
     [Google Scholar]
  46. Liu W, Duns G, Chen J. Genomic characterization of a novel partitivirus infecting Aspergillus ochraceus. Virus Genes 2008; 37:322–327 [View Article] [PubMed]
     [Google Scholar]
  47. Vainio EJ, Chiba S, Ghabrial SA, Maiss E, Roossinck M et al. ICTV Virus Taxonomy Profile: Partitiviridae. . J Gen Virol 2018; 99:17–18 [View Article] [PubMed]
     [Google Scholar]
  48. Cross ST, Maertens BL, Dunham TJ, Rodgers CP, Brehm AL et al. Partitiviruses infecting Drosophila melanogaster and Aedes aegypti exhibit efficient biparental vertical transmission. J Virol 2020; 94:01070–20 [View Article] [PubMed]
     [Google Scholar]
  49. Nerva L, Silvestri A, Ciuffo M, Palmano S, Varese GC et al. Transmission of Penicillium aurantiogriseum partiti-like virus 1 to a new fungal host (Cryphonectria parasitica) confers higher resistance to salinity and reveals adaptive genomic changes. Environ Microbiol 2017; 19:4480–4492 [View Article] [PubMed]
     [Google Scholar]
  50. Nerva L, Chitarra W, Siciliano I, Gaiotti F, Ciuffo M et al. Mycoviruses mediate mycotoxin regulation in Aspergillus ochraceus. Environ Microbiol 2019; 21:1957–1968 [View Article] [PubMed]
     [Google Scholar]
  51. Chun J, Yang H-E, Kim D-H. Identification of a novel partitivirus of Trichoderma harzianum NFCF319 and evidence for the related antifungal activity. Front Plant Sci 2018; 9:1699 [View Article] [PubMed]
     [Google Scholar]
  52. Xiao X, Cheng J, Tang J, Fu Y, Jiang D et al. A novel partitivirus that confers hypovirulence on plant pathogenic fungi. J Virol 2014; 88:10120–10133 [View Article] [PubMed]
     [Google Scholar]
  53. Telengech P, Hisano S, Mugambi C, Hyodo K, Arjona-López JM et al. Diverse partitiviruses from the phytopathogenic fungus, Rosellinia necatrix. Front Microbiol 2020; 11:1064 [View Article] [PubMed]
     [Google Scholar]
  54. Li Y, Li S, Liang Z, Cai Q, Zhou T et al. RNA-seq analysis of Rhizoctonia solani AG-4HGI strain BJ-1H infected by a new viral strain of Rhizoctonia solani partitivirus 2 reveals a potential mechanism for hypovirulence. Phytopathology 2022; 112:1373–1385 [View Article] [PubMed]
     [Google Scholar]
  55. Vainio EJ, Jurvansuu J, Hyder R, Kashif M, Piri T et al. Heterobasidion partitivirus 13 mediates severe growth debilitation and major alterations in the gene expression of a fungal forest pathogen. J Virol 2018; 92:e01744–17 [View Article] [PubMed]
     [Google Scholar]
  56. Kotta-Loizou I, Coutts RHA. Mycoviruses in Aspergilli: a comprehensive review. Front Microbiol 2017; 8:1699 [View Article] [PubMed]
     [Google Scholar]
  57. Magae Y, Sunagawa M. Characterization of a mycovirus associated with the brown discoloration of edible mushroom, Flammulina velutipes. Virol J 2010; 7:1–8 [View Article] [PubMed]
     [Google Scholar]
  58. Bhatti MF, Jamal A, Petrou MA, Cairns TC, Bignell EM et al. The effects of dsRNA mycoviruses on growth and murine virulence of Aspergillus fumigatus. Fungal Genet Biol 2011; 48:1071–1075 [View Article] [PubMed]
     [Google Scholar]
  59. Zheng L, Zhang M, Chen Q, Zhu M, Zhou E. A novel mycovirus closely related to viruses in the genus Alphapartitivirus confers hypovirulence in the phytopathogenic fungus Rhizoctonia solani. Virology 2014; 456–457:220–226 [View Article] [PubMed]
     [Google Scholar]
  60. Jom-in S, Akarapisan A. Characterization of double-stranded RNA in Trichoderma spp. isolates in Chiang mai province. J Agric Technol 2009; 5:261–270
     [Google Scholar]
  61. Liu C, Li M, Redda ET, Mei J, Zhang J et al. A novel double-stranded RNA mycovirus isolated from Trichoderma harzianum. Virol J 2019; 16:1–10 [View Article] [PubMed]
     [Google Scholar]
  62. Suárez-Estrella F, Arcos-Nievas MA, López MJ, Vargas-García MC, Moreno J. Biological control of plant pathogens by microorganisms isolated from agro-industrial composts. Biol Control 2013; 67:509–515 [View Article]
     [Google Scholar]
  63. Anis M, Abbasi MW, Zaki MJ. Bioefficacy of microbial antagonists against Macrophomina phaseolina on sunflower. Pak J Bot 2010; 42:2935–2940
     [Google Scholar]
/content/journal/jgv/10.1099/jgv.0.001925
Loading
Molecular and biological characterization of a partitivirus from Paecilomyces variotii
J. Gen. Virol. 104, 001925 (2023); https://doi.org/10.1099/jgv.0.001925
/content/journal/jgv/10.1099/jgv.0.001925
/content/journal/jgv/10.1099/jgv.0.001925
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error