Hiding in plain sight: New virus genomes discovered via a systematic analysis of fungal public transcriptomes

Abstract

The distribution and diversity of RNA viruses in fungi is incompletely understood due to the often cryptic nature of mycoviral infections and the focused study of primarily pathogenic and/or economically important fungi. As most viruses that are known to infect fungi possess either single-stranded or double-stranded RNA genomes, transcriptomic data provides the opportunity to query for viruses in diverse fungal samples without any a priori knowledge of virus infection. Here we describe a systematic survey of all transcriptomic datasets from fungi belonging to the subphylum Pezizomycotina. Using a simple but effective computational pipeline that uses reads discarded during normal RNA-seq analyses, followed by identification of a viral RNA-dependent RNA polymerase (RdRP) motif in de novo assembled contigs, 59 viruses from 44 different fungi were identified. Among the viruses identified, 88% were determined to be new species and 68% are, to our knowledge, the first virus described from the fungal species. Comprehensive analyses of both nucleotide and inferred protein sequences characterize the phylogenetic relationships between these viruses and the known set of mycoviral sequences and support the classification of up to four new families and two new genera. Thus the results provide a deeper understanding of the scope of mycoviral diversity while also increasing the distribution of fungal hosts. Further, this study demonstrates the suitability of analyzing RNA-seq data to facilitate rapid discovery of new viruses.

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    Not in our library10.1016/j.virol.2017.03.003

92. 92.

    Donaire L, Rozas J, Ayllón MA. Molecular characterization of Botrytis ourmia-like virus, a mycovirus close to the plant pathogenic genus Ourmiavirus. Virology. 2016;489: 158–164.

    Not in our library10.1016/j.virol.2015.11.027

93. 93.

    Suzuki N, Ghabrial SA, Kim K-H, Pearson M, Marzano S-YL, Yaegashi H, et al ICTV Virus Taxonomy Profile: Hypoviridae. J Gen Virol. 2018;99: 615–616.

    Not in our library10.1099/jgv.0.001055

94. 94.

    Fahima T, Kazmierczak P, Hansen DR, Pfeiffer P, Van Alfen NK. Membrane-associated replication of an unencapsidated double-strand RNA of the fungus, Cryphonectria parasitica. Virology. 1993;195: 81–89.

    Not in our library10.1006/viro.1993.1348

95. 95.

    Jacob-Wilk D, Turina M, Van Alfen NK. Mycovirus cryphonectria hypovirus 1 elements cofractionate with trans-Golgi network membranes of the fungal host Cryphonectria parasitica. J Virol. 2006;80: 6588–6596.

    Not in our library10.1128/jvi.02519-05

96. 96.

    Li P, Zhang H, Chen X, Qiu D, Guo L. Molecular characterization of a novel hypovirus from the plant pathogenic fungus Fusarium graminearum. Virology. 2015;481: 151–160.

    Not in our library10.1016/j.virol.2015.02.047

97. 97.

    Yaegashi H, Kanematsu S, Ito T. Molecular characterization of a new hypovirus infecting a phytopathogenic fungus, Valsa ceratosperma. Virus Res. 2012;165: 143–150.

    Not in our library10.1016/j.virusres.2012.02.008

98. 98.

    Shapira R, Choi GH, Nuss DL. Virus-like genetic organization and expression strategy for a double-stranded RNA genetic element associated with biological control of chestnut blight. EMBO J. 1991;10: 731–739. Available: https://www.ncbi.nlm.nih.gov/pubmed/2009854

    Not in our library10.1002/j.1460-2075.1991.tb08004.x

99. 99.

    Hillman BI, Halpern BT, Brown MP. A viral dsRNA element of the chestnut blight fungus with a distinct genetic organization. Virology. 1994;201: 241–250.

    Not in our library10.1006/viro.1994.1289

100. 100.

     Arjona-Lopez JM, Telengech P, Jamal A, Hisano S, Kondo H, Yelin MD, et al Novel, diverse RNA viruses from Mediterranean isolates of the phytopathogenic fungus, Rosellinia necatrix: insights into evolutionary biology of fungal viruses. Environ Microbiol. 2018;20: 1464–1483.

     Not in our library10.1111/1462-2920.14065

101. 101.

     Li P, Chen X, He H, Qiu D, Guo L. Complete Genome Sequence of a Novel Hypovirus from the Phytopathogenic Fungus Fusarium langsethiae. Genome Announc. 2017;5

     Not in our library10.1128/genomea.01722-16

102. 102.

     Zhang R, Liu S, Chiba S, Kondo H, Kanematsu S, Suzuki N. A novel single-stranded RNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix, with similarity to hypo-like viruses. Front Microbiol. 2014;5: 360

     Not in our library10.3389/fmicb.2014.00360

103. 103.

     Hrabáková L, Grum-Grzhimaylo AA, Koloniuk I, Debets AJM, Sarkisova T, Petrzik K. The alkalophilic fungus Sodiomyces alkalinus hosts beta- and gammapartitiviruses together with a new fusarivirus. PLoS One. 2017;12: e0187799

     Not in our library10.1371/journal.pone.0187799

104. 104.

     Liu R, Cheng J, Fu Y, Jiang D, Xie J. Molecular Characterization of a Novel Positive-Sense, Single-Stranded RNA Mycovirus Infecting the Plant Pathogenic Fungus Sclerotinia sclerotiorum. Viruses. 2015;7: 2470–2484.

     Not in our library10.3390/v7052470

105. 105.

     Liu H, Fu Y, Jiang D, Li G, Xie J, Peng Y, et al A novel mycovirus that is related to the human pathogen hepatitis E virus and rubi-like viruses. J Virol. 2009;83: 1981–1991.

     Not in our library10.1128/jvi.01897-08

106. 106.

     Bartholomäus A, Wibberg D, Winkler A, Pühler A, Schlüter A, Varrelmann M. Deep Sequencing Analysis Reveals the Mycoviral Diversity of the Virome of an Avirulent Isolate of Rhizoctonia solani AG-2-2 IV. PLoS One. 2016;11: e0165965

     Not in our library10.1371/journal.pone.0165965

107. 107.

     Koonin EV, Dolja VV, Krupovic M. Origins and evolution of viruses of eukaryotes: The ultimate modularity. Virology. 2015;479–480: 2–25.

     Not in our library10.1016/j.virol.2015.02.039

108. 108.
     Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi · 2016

     Corrected
109. 109.

     Grandaubert J, Bhattacharyya A, Stukenbrock EH. RNA-seq-Based Gene Annotation and Comparative Genomics of Four Fungal Grass Pathogens in the Genus Zymoseptoria Identify Novel Orphan Genes and Species-Specific Invasions of Transposable Elements. G3. 2015;5: 1323–1333.

     Not in our library10.1534/g3.115.017731

110. 110.

     Rajakaruna P, Khandekar S, Meulia T, Leisner SM. Identification and Host Relations of Turnip ringspot virus, A Novel Comovirus from Ohio. Plant Dis. Scientific Societies; 2007;91: 1212–1220.

     Not in our library10.1094/pdis-91-10-1212

111. 111.

     Roossinck MJ. The good viruses: viral mutualistic symbioses. Nat Rev Microbiol. 2011;9: 99–108.

     Not in our library10.1038/nrmicro2491

112. 112.

     Schmitt MJ, Breinig F. The viral killer system in yeast: from molecular biology to application. FEMS Microbiol Rev. 2002;26: 257–276. Available: https://www.ncbi.nlm.nih.gov/pubmed/12165427

     Not in our library10.1111/j.1574-6976.2002.tb00614.x

113. 113.

     Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science. 2007;315: 513–515.

     Not in our library10.1126/science.1136237

114. 114.

     Niu Y, Yuan Y, Mao J, Yang Z, Cao Q, Zhang T, et al Characterization of two novel mycoviruses from Penicillium digitatum and the related fungicide resistance analysis. Sci Rep. 2018;8: 5513

     Not in our library10.1038/s41598-018-23807-3

115. 115.

     Chiba S, Suzuki N. Highly activated RNA silencing via strong induction of dicer by one virus can interfere with the replication of an unrelated virus. Proc Natl Acad Sci U S A. 2015;112: E4911–8.

     Not in our library10.1073/pnas.1509151112

116. 116.

     Segers GC, Zhang X, Deng F, Sun Q, Nuss DL. Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proc Natl Acad Sci U S A. 2007;104: 12902–12906.

     Not in our library10.1073/pnas.0702500104

117. 117.

     Mochama P, Jadhav P, Neupane A, Lee Marzano S-Y. Mycoviruses as Triggers and Targets of RNA Silencing in White Mold Fungus Sclerotinia sclerotiorum. Viruses. 2018;10

     Not in our library10.3390/v10040214

118. 118.

     Kirk PM, Cannon PF, David JC, Stalpers JA, editor. Ainsworth and Bisby’s Dictionary of Fungi. CABI Bioscience; 2001.

     Not in our library

119. 119.

     Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9: 357–359.

     Not in our library10.1038/nmeth.1923

120. 120.

     Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8: 1494–1512.

     Not in our library10.1038/nprot.2013.084

121. 121.

     TransDecoder WebCitation [Internet]. [cited 16 Aug 2017]. Available: transdecoder.github.io

     Not in our library

122. 122.

     HMMER [Internet]. [cited 14 Jun 2018]. Available: http://hmmer.org

     Not in our library

123. 123.

     Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011;17: 10–12.

     Not in our library10.14806/ej.17.1.200

124. 124.

     Home - ORFfinder - NCBI [Internet]. [cited 20 Dec 2017]. Available: https://www.ncbi.nlm.nih.gov/orffinder/

     Not in our library

125. 125.

     SankeyMATIC (BETA): A Sankey diagram builder for everyone [Internet]. [cited 14 Jun 2018]. Available: http://sankeymatic.com/

     Not in our library

126. 126.

     Sperschneider J, Datta A. DotKnot: pseudoknot prediction using the probability dot plot under a refined energy model. Nucleic Acids Res. 2010;38: e103

     Not in our library10.1093/nar/gkq021

127. 127.

     Sperschneider J, Datta A, Wise MJ. Heuristic RNA pseudoknot prediction including intramolecular kissing hairpins. RNA. 2011;17: 27–38.

     Not in our library10.1261/rna.2394511

128. 128.

     Byun Y, Han K. PseudoViewer3: generating planar drawings of large-scale RNA structures with pseudoknots. Bioinformatics. 2009;25: 1435–1437.

     Not in our library10.1093/bioinformatics/btp252

129. 129.

     Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30: 772–780.

     Not in our library10.1093/molbev/mst010

130. 130.

     Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25: 1972–1973.

     Not in our library10.1093/bioinformatics/btp348

131. 131.

     Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22: 2688–2690.

     Not in our library10.1093/bioinformatics/btl446

132. 132.

     Huson DH, Scornavacca C. Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst Biol. 2012;61: 1061–1067.

     Not in our library10.1093/sysbio/sys062

133. 133.

     Li W, Cowley A, Uludag M, Gur T, McWilliam H, Squizzato S, et al The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Res. 2015;43: W580–4.

     Not in our library10.1093/nar/gkv279

Cited by papers we hold 3

• Novel Mycoviruses Discovered in the Mycovirome of a Necrotrophic Fungus · 2021
  Not checked
• Establishment of Neurospora crassa as a model organism for fungal virology · 2020
  Not checked
• Abundant and Diverse RNA Viruses in Insects Revealed by RNA-Seq Analysis: Ecological and Evolutionary Implications · 2020
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.