Re-assessing the diversity of negative strand RNA viruses in insects

English version

Autoři: Simon Käfer ^aff001; Sofia Paraskevopoulou ^aff001; Florian Zirkel ^aff003; Nicolas Wieseke ^aff004; Alexander Donath ^aff002; Malte Petersen ^aff005; Terry C. Jones ^aff001; Shanlin Liu ^aff007; Xin Zhou ^aff008; Martin Middendorf ^aff004; Sandra Junglen ^aff001; Bernhard Misof ^aff002; Christian Drosten ^aff001
Působiště autorů: Institute of Virology, Charité-Universitätsmedizin Berlin, Corporate Member of Free University, Humboldt-University and Berlin Institute of Health, Berlin, Germany ^aff001; Center for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Bonn, Germany ^aff002; Institute of Virology, University of Bonn Medical Centre, Bonn, Germany ^aff003; Swarm Intelligence and Complex Systems Group, Department of Computer Science, Leipzig University, Germany ^aff004; Senckenberg Biodiversity and Climate Research Centre, Senckenberg Gesellschaft für Naturforschung, Frankfurt am Main, Germany ^aff005; Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge, United Kingdom ^aff006; BGI-Shenzhen, China Beishan Industrial Zone, Shenzhen, Guangdong Province, China ^aff007; College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, China ^aff008; Beijing Advanced Innovation Center for Food Nutrition and Human Health, China Agricultural University, Beijing, China ^aff009; German Center for Infection Research (DZIF), associated partner site Charité, Berlin, Germany ^aff010
Vyšlo v časopise: Re-assessing the diversity of negative strand RNA viruses in insects. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008224
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008224

Souhrn

The spectrum of viruses in insects is important for subjects as diverse as public health, veterinary medicine, food production, and biodiversity conservation. The traditional interest in vector-borne diseases of humans and livestock has drawn the attention of virus studies to hematophagous insect species. However, these represent only a tiny fraction of the broad diversity of Hexapoda, the most speciose group of animals. Here, we systematically probed the diversity of negative strand RNA viruses in the largest and most representative collection of insect transcriptomes from samples representing all 34 extant orders of Hexapoda and 3 orders of Entognatha, as well as outgroups, altogether representing 1243 species. Based on profile hidden Markov models we detected 488 viral RNA-directed RNA polymerase (RdRp) sequences with similarity to negative strand RNA viruses. These were identified in members of 324 arthropod species. Selection for length, quality, and uniqueness left 234 sequences for analyses, showing similarity to genomes of viruses classified in Bunyavirales (n = 86), Articulavirales (n = 54), and several orders within Haploviricotina (n = 94). Coding-complete genomes or nearly-complete subgenomic assemblies were obtained in 61 cases. Based on phylogenetic topology and the availability of coding complete genomes we estimate that at least 20 novel viral genera in seven families need to be defined, only two of them monospecific. Seven additional viral clades emerge when adding sequences from the present study to formerly monospecific lineages, potentially requiring up to seven additional genera. One long sequence may indicate a novel family. For segmented viruses, cophylogenies between genome segments were generally improved by the inclusion of viruses from the present study, suggesting that in silico misassembly of segmented genomes is rare or absent. Contrary to previous assessments, significant virus-host codivergence was identified in major phylogenetic lineages based on two different approaches of codivergence analysis in a hypotheses testing framework. In spite of these additions to the known spectrum of viruses in insects, we caution that basing taxonomic decisions on genome information alone is challenging due to technical uncertainties, such as the inability to prove integrity of complete genome assemblies of segmented viruses.

Klíčová slova:

Animal phylogenetics – Insects – Invertebrate genomics – Phylogenetic analysis – Phylogenetics – Taxonomy – Viral genomics – Viral taxonomy

Zdroje

1. Claas ECJ, Osterhaus AD, van Beek R, De Jong JC, Rimmelzwaan GF, Senne DA, et al. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet. 1998;351(9101):472–7. doi: 10.1016/S0140-6736(97)11212-0 9482438

2. Drexler JF, Corman VM, Müller MA, Maganga GD, Vallo P, Binger T, et al. Bats host major mammalian paramyxoviruses. Nat Commun. 2012;3:796. doi: 10.1038/ncomms1796 22531181

3. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. Global trends in emerging infectious diseases. Nature. 2008;451:990–3. doi: 10.1038/nature06536 18288193

4. Li C-X, Shi M, Tian J-H, Lin X-D, Kang Y-J, Chen L-J, et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife. 2015;4. doi: 10.7554/eLife.05378 25633976

5. Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, et al. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346(6210):763–7. doi: 10.1126/science.1257570 25378627

6. Shi M, Lin X-D, Chen X, Tian J-H, Chen L-J, Li K, et al. The evolutionary history of vertebrate RNA viruses. Nature. 2018;556(7700):197–202. doi: 10.1038/s41586-018-0012-7 29618816

7. Junglen S, Drosten C. Virus discovery and recent insights into virus diversity in arthropods. Curr Opin Microbiol. 2013;16(4):507–13. doi: 10.1016/j.mib.2013.06.005 23850098

8. Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X, Li C-X, et al. Redefining the invertebrate RNA virosphere. Nature. 2016;540(7634):539–43. doi: 10.1038/nature20167 27880757

9. Simmonds P, Adams MJ, Benkő M, Breitbart M, Brister JR, Carstens EB, et al. Virus taxonomy in the age of metagenomics. Nature Reviews Microbiology. 2017;15:161. doi: 10.1038/nrmicro.2016.177

10. Wignall-Fleming EB, Hughes DJ, Vattipally S, Modha S, Goodbourn S, Davison AJ, et al. Analysis of Paramyxovirus Transcription and Replication by High-Throughput Sequencing. J Virol. 2019;93(17). Epub 2019/06/14. doi: 10.1128/jvi.00571-19 31189700; PubMed Central PMCID: PMC6694822.

11. Di Giallonardo F, Audsley MD, Shi M, Young PR, McGraw EA, Holmes EC. Complete genome of Aedes aegypti anphevirus in the Aag2 mosquito cell line. Journal of General Virology. 2018;99(6):832–6. doi: 10.1099/jgv.0.001079 29741476

12. Schoonvaere K, De Smet L, Smagghe G, Vierstraete A, Braeckman BP, de Graaf DC. Unbiased RNA Shotgun Metagenomics in Social and Solitary Wild Bees Detects Associations with Eukaryote Parasites and New Viruses. PLoS One. 2016;11(12):e0168456. doi: 10.1371/journal.pone.0168456 28006002

13. Wolf YI, Kazlauskas D, Iranzo J, Lucia-Sanz A, Kuhn JH, Krupovic M, et al. Origins and Evolution of the Global RNA Virome. MBio. 2018;9(6). Epub 2018/11/30. doi: 10.1128/mBio.02329-18 30482837; PubMed Central PMCID: PMC6282212.

14. Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30(9):1236–40. doi: 10.1093/bioinformatics/btu031 24451626

15. Elliott RM. Molecular biology of the Bunyaviridae. J Gen Virol. 1990;71 (Pt 3):501–22. doi: 10.1099/0022-1317-71-3-501 2179464

16. Mir MA, Brown B, Hjelle B, Duran WA, Panganiban AT. Hantavirus N protein exhibits genus-specific recognition of the viral RNA panhandle. J Virol. 2006;80(22):11283–92. doi: 10.1128/JVI.00820-06 16971445

17. Conow C, Fielder D, Ovadia Y, Libeskind-Hadas R. Jane: a new tool for the cophylogeny reconstruction problem. Algorithms Mol Biol. 2010;5:16. doi: 10.1186/1748-7188-5-16 20181081

18. Merkle D, Middendorf M, Wieseke N. A parameter-adaptive dynamic programming approach for inferring cophylogenies. BMC Bioinformatics. 2010;11 Suppl 1:S60. doi: 10.1186/1471-2105-11-S1-S60 20122236

19. Halloran A, Vantomme P, Hanboonsong Y, Ekesi S. Regulating edible insects: the challenge of addressing food security, nature conservation, and the erosion of traditional food culture. Food Security. 2015;7(3):739–46. doi: 10.1007/s12571-015-0463-8

20. Makhsous N, Shean RC, Droppers D, Guan J, Jerome KR, Greninger AL. Genome Sequences of Three Novel Bunyaviruses, Two Novel Rhabdoviruses, and One Novel Nyamivirus from Washington State Moths. Genome Announc. 2017;5(7). doi: 10.1128/genomeA.01668-16 28209840

21. Marklewitz M, Zirkel F, Rwego IB, Heidemann H, Trippner P, Kurth A, et al. Discovery of a unique novel clade of mosquito-associated bunyaviruses. J Virol. 2013;87(23):12850–65. doi: 10.1128/JVI.01862-13 24067954

22. Bergsten J. A review of long-branch attraction. Cladistics. 2005;21(2):163–93.

23. Wiens JJ. Can incomplete taxa rescue phylogenetic analyses from long-branch attraction? Syst Biol. 2005;54(5):731–42. doi: 10.1080/10635150500234583 16243761

24. Obbard DJ. Expansion of the metazoan virosphere: Progress, pitfalls, and prospects. Current opinion in virology. 2018;31:17–23. doi: 10.1016/j.coviro.2018.08.008 30237139

25. Maes P, Song T, Mark S, Paweska J, Song Q, Ye G, et al. ICTV taxonomic report 2017.016M.R.: Taxonomic expansion and reorganization of the order Mononegavirales.

26. Maes P, Alkhovsky S, Beer M, Briese T, Buchmeier MJ, Calisher CH, et al. ICTV taxonomic proposal 2017.012M: Taxonomic expansion and reorganization of the order Bunyavirales.

27. Lauber C, Gorbalenya AE. Partitioning the genetic diversity of a virus family: approach and evaluation through a case study of picornaviruses. J Virol. 2012;86(7):3890–904. doi: 10.1128/JVI.07173-11 22278230

28. Simmonds P. Methods for virus classification and the challenge of incorporating metagenomic sequence data. J Gen Virol. 2015;96(Pt 6):1193–206. doi: 10.1099/jgv.0.000016 26068186

29. Schuster S, Zirkel F, Kurth A, van Cleef KWR, Drosten C, van Rij RP, et al. A Unique Nodavirus with Novel Features: Mosinovirus Expresses Two Subgenomic RNAs, a Capsid Gene of Unknown Origin, and a Suppressor of the Antiviral RNA Interference Pathway. Journal of Virology. 2014;88(22):13447–59. doi: 10.1128/JVI.02144-14 25210176

30. Aiewsakun P, Adriaenssens EM, Lavigne R, Kropinski AM, Simmonds P. Evaluation of the genomic diversity of viruses infecting bacteria, archaea and eukaryotes using a common bioinformatic platform: steps towards a unified taxonomy. J Gen Virol. 2018;99:1331–43. doi: 10.1099/jgv.0.001110 30016225

31. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 2010;20(2):265–72. doi: 10.1101/gr.097261.109 20019144

32. Notredame C, Higgins DG, Heringa J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol. 2000;302(1):205–17. doi: 10.1006/jmbi.2000.4042 10964570

33. Slater GSC, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics. 2005;6:31. doi: 10.1186/1471-2105-6-31 15713233

34. Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol. 2011;7(10):e1002195. doi: 10.1371/journal.pcbi.1002195 22039361

35. Katoh K, Misawa K, Kuma K-I, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059–66. doi: 10.1093/nar/gkf436 12136088

36. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25(15):1972–3. doi: 10.1093/bioinformatics/btp348 19505945

37. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. doi: 10.1093/sysbio/syq010 20525638

38. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421. doi: 10.1186/1471-2105-10-421 20003500

39. Contreras MA, Eastwood G, Guzman H, Popov V, Savit C, Uribe S, et al. Almendravirus: A Proposed New Genus of Rhabdoviruses Isolated from Mosquitoes in Tropical Regions of the Americas. Am J Trop Med Hyg. 2017;96:100–9. doi: 10.4269/ajtmh.16-0403 27799634

40. Reuter G, Boros Á, Pál J, Kapusinszky B, Delwart E, Pankovics P. Detection and genome analysis of a novel (dima)rhabdovirus (Riverside virus) from Ochlerotatus sp. mosquitoes in Central Europe. Infect Genet Evol. 2016;39:336–41. doi: 10.1016/j.meegid.2016.02.016 26883377

41. Shahhosseini N, Lühken R, Jöst H, Jansen S, Börstler J, Rieger T, et al. Detection and characterization of a novel rhabdovirus in Aedes cantans mosquitoes and evidence for a mosquito-associated new genus in the family Rhabdoviridae. Infect Genet Evol. 2017;55:260–8. doi: 10.1016/j.meegid.2017.09.026 28943405

42. Sun Q, Zhao Q, An X, Guo X, Zuo S, Zhang X, et al. Complete genome sequence of Menghai rhabdovirus, a novel mosquito-borne rhabdovirus from China. Arch Virol. 2017;162:1103–6. doi: 10.1007/s00705-016-3188-x 28000049

43. Tokarz R, Sameroff S, Tagliafierro T, Jain K, Williams SH, Cucura DM, et al. Identification of Novel Viruses in Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis Ticks. mSphere. 2018;3. doi: 10.1128/mSphere.00614-17 29564401

44. Xu CL, Cantalupo PG, Sáenz-Robles MT, Baldwin A, Fitzpatrick D, Norris DE, et al. Draft Genome Sequence of a Novel Rhabdovirus Isolated from Deinocerites Mosquitoes. Genome Announc. 2018;6. doi: 10.1128/genomeA.01438-17 29748415

45. Axén C, Hakhverdyan M, Boutrup TS, Blomkvist E, Ljunghager F, Alfjorden A, et al. Emergence of a new rhabdovirus associated with mass mortalities in eelpout (Zoarces viviparous) in the Baltic Sea. J Fish Dis. 2017;40:219–29. doi: 10.1111/jfd.12506 27416895

46. Charles J, Firth AE, Loroño-Pino MA, Garcia-Rejon JE, Farfan-Ale JA, Lipkin WI, et al. Merida virus, a putative novel rhabdovirus discovered in Culex and Ochlerotatus spp. mosquitoes in the Yucatan Peninsula of Mexico. J Gen Virol. 2016;97:977–87. doi: 10.1099/jgv.0.000424 26868915

47. Cholleti H, Hayer J, Abilio AP, Mulandane FC, Verner-Carlsson J, Falk KI, et al. Discovery of Novel Viruses in Mosquitoes from the Zambezi Valley of Mozambique. PLoS One. 2016;11:e0162751. doi: 10.1371/journal.pone.0162751 27682810

48. Lara Pinto AZd, Santos de Carvalho M, de Melo FL, Ribeiro ALM, Morais Ribeiro B, Dezengrini Slhessarenko R. Novel viruses in salivary glands of mosquitoes from sylvatic Cerrado, Midwestern Brazil. PLoS One. 2017;12:e0187429. doi: 10.1371/journal.pone.0187429 29117239

49. Økland AL, Nylund A, Øvergård A-C, Blindheim S, Watanabe K, Grotmol S, et al. Genomic characterization and phylogenetic position of two new species in Rhabdoviridae infecting the parasitic copepod, salmon louse (Lepeophtheirus salmonis). PLoS One. 2014;9:e112517. doi: 10.1371/journal.pone.0112517 25402203

50. Sabbadin F, Glover R, Stafford R, Rozado-Aguirre Z, Boonham N, Adams I, et al. Transcriptome sequencing identifies novel persistent viruses in herbicide resistant wild-grasses. Sci Rep. 2017;7:41987. doi: 10.1038/srep41987 28165016

51. Shi M, Neville P, Nicholson J, Eden J-S, Imrie A, Holmes EC. High-Resolution Metatranscriptomics Reveals the Ecological Dynamics of Mosquito-Associated RNA Viruses in Western Australia. J Virol. 2017;91. doi: 10.1128/JVI.00680-17 28637756

52. Simo Tchetgna HD, Nakoune E, Selekon B, Gessain A, Manuguerra J-C, Kazanji M, et al. Molecular Characterization of the Kamese Virus, an Unassigned Rhabdovirus, Isolated from Culex pruina in the Central African Republic. Vector Borne Zoonotic Dis. 2017;17:447–51. doi: 10.1089/vbz.2016.2068 28350284

53. Coffey LL, Page BL, Greninger AL, Herring BL, Russell RC, Doggett SL, et al. Enhanced arbovirus surveillance with deep sequencing: Identification of novel rhabdoviruses and bunyaviruses in Australian mosquitoes. Virology. 2014;448:146–58. doi: 10.1016/j.virol.2013.09.026 24314645

54. Contreras-Gutiérrez MA, Nunes MRT, Guzman H, Uribe S, Suaza Vasco JD, Cardoso JF, et al. Sinu virus, a novel and divergent orthomyxovirus related to members of the genus Thogotovirus isolated from mosquitoes in Colombia. Virology. 2017;501:166–75. doi: 10.1016/j.virol.2016.11.014 27936462

55. Ejiri H, Lim C-K, Isawa H, Fujita R, Murota K, Sato T, et al. Characterization of a novel thogotovirus isolated from Amblyomma testudinarium ticks in Ehime, Japan: A significant phylogenetic relationship to Bourbon virus. Virus Res. 2018;249:57–65. doi: 10.1016/j.virusres.2018.03.004 29548745

56. Medd NC, Fellous S, Waldron FM, Xuéreb A, Nakai M, Cross JV, et al. The virome of Drosophila suzukii, an invasive pest of soft fruit. Virus Evol. 2018;4:vey009. doi: 10.1093/ve/vey009 29644097

57. Rodrigues DSG, Medeiros DBdA, Rodrigues SG, Martins LC, de Lima CPS, de Oliveira LF, et al. Pacui Virus, Rio Preto da Eva Virus, and Tapirape Virus, Three Distinct Viruses within the Family Bunyaviridae. Genome Announc. 2014;2. doi: 10.1128/genomeA.00923-14 25395627

58. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: A fast, scalable, and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics. 2019;35(21):4453–5. doi: 10.1093/bioinformatics/btz305 31070718

59. Lemoine F, B. Domelevo Entfellner J, Wilkinson E, Correia D, Dávila Felipe M, De Oliveira T, et al. Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature. 2018;556(7702):452–6. doi: 10.1038/s41586-018-0043-0 29670290

60. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–42. doi: 10.1093/sysbio/sys029 22357727

61. Yu G, Smith DK, Zhu H, Guan Y, Lam TT-Y. ggtree: anrpackage for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol. 2016;8(1):28–36. doi: 10.1111/2041-210x.12628

62. Galili T. dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering. Bioinformatics. 2015;31(22):3718–20. doi: 10.1093/bioinformatics/btv428 26209431

63. Arnholt AT, Evans B. BSDA: Basic Statistics and Data Analysis. 2017.