Novel partiti-like viruses are conditional mutualistic symbionts in their normal lepidopteran host, African armyworm, but parasitic in a novel host, Fall armyworm

English version

Autoři: Pengjun Xu ^aff001; Liyu Yang ^aff001; Xianming Yang ^aff003; Tong Li ^aff004; Robert I. Graham ^aff005; Kongming Wu ^aff003; Kenneth Wilson ^aff002
Působiště autorů: Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ^aff001; Lancaster Environment Centre, Lancaster University, Lancaster, United Kingdom ^aff002; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China ^aff003; Institute of Plant Protection, Henan Academy of Agricultural Sciences, Zhengzhou, China ^aff004; Department of Animal and Agriculture, Hartpury University, Gloucester, United Kingdom ^aff005
Vyšlo v časopise: Novel partiti-like viruses are conditional mutualistic symbionts in their normal lepidopteran host, African armyworm, but parasitic in a novel host, Fall armyworm. PLoS Pathog 16(6): e32767. doi:10.1371/journal.ppat.1008467
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008467

Souhrn

Recent advances in next generation sequencing (NGS) (e.g. metagenomic and transcriptomic sequencing) have facilitated the discovery of a large number of new insect viruses, but the characterization of these viruses is still in its infancy. Here, we report the discovery, using RNA-seq, of three new partiti-like viruses from African armyworm, Spodoptera exempta (Lepidoptera: Noctuidae), which are all vertically-transmitted transovarially from mother to offspring with high efficiency. Experimental studies show that the viruses reduce their host’s growth rate and reproduction, but enhance their resistance to a nucleopolyhedrovirus (NPV). Via microinjection, these partiti-like viruses were transinfected into a novel host, a newly-invasive crop pest in sub-Saharan Africa (SSA), the Fall armyworm, S. frugiperda. This revealed that in this new host, these viruses appear to be deleterious without any detectable benefit; reducing their new host’s reproductive rate and increasing their susceptibility to NPV. Thus, the partiti-like viruses appear to be conditional mutualistic symbionts in their normal host, S. exempta, but parasitic in the novel host, S. frugiperda. Transcriptome analysis of S. exempta and S. frugiperda infected, or not, with the partiti-like viruses indicates that the viruses may regulate pathways related to immunity and reproduction. These findings suggest a possible pest management strategy via the artificial host-shift of novel viruses discovered by NGS.

Klíčová slova:

Host-pathogen interactions – Larvae – Microinjection – Pupae – RNA viruses – Viral gene expression – Viral transmission and infection – Spodoptera

Zdroje

1. Shi M, Lin X, Tian J, Chen L, Chen X, Li C, et al. Redefining the invertebrate RNA virosphere. Nature. 2016; 540(7634): 539–543. doi: 10.1038/nature20167 27880757

2. Shi M, Lin X, Chen X, Tian J, Chen L, 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

3. Shi M, White VL, Schlub T, Eden JS, Hoffmann AA, Holmes EC. No detectable effect of Wolbachia wMel on the prevalence and abundance of the RNA virome of Drosophila melanogaster. Proc Biol Sci. 2018; 285(1883): 20181165. doi: 10.1098/rspb.2018.1165 30051873

4. Käfer S, Paraskevopoulou S, Zirkel F, Wieseke N, Donath A, Peterson M, et al. Re-assessing the diversity of negative strand RNA viruses in insects. PLoS Pathog. 2019; 15(12): e1008224. doi: 10.1371/journal.ppat.1008224 31830128

5. Webster CL, Waldron FM, Robertson S, Crowson D, Ferrari G, Quintana JF, et al. The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLoS Biol. 2015; 13(7): e1002210. doi: 10.1371/journal.pbio.1002210 26172158

6. Haase S, Sciocco-Cap A, Romanowski V. Baculovirus insecticides in Latin America: historical overview, current status and future perspectives. Viruses. 2015; 7(5): 2230–2267. doi: 10.3390/v7052230 25941826

7. Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS. Insect pathogens as biological control agents: Back to the future. J Invertebr Pathol. 2015; 132(Nov 2015): 1–41. doi: 10.1016/j.jip.2015.07.009 26225455

8. Winstanley D, Rovesti L. Insect viruses as biocontrol agents. In: Jones DG, editor. Exploitation of Microorganisms. Dordrecht: Springer; 1993. p. 105–136.

9. Graham RI, Grzywacz D, Mushobozi WL, Wilson K. Wolbachia in a major African crop pest increases susceptibility to viral disease rather than protects. Ecol Lett. 2012; 15(9): 993–1000. doi: 10.1111/j.1461-0248.2012.01820.x 22731846

10. Clem RJ, Passarelli AL. Baculoviruses: sophisticated pathogens of insects. PLoS Pathog. 2013; 9(11): e1003729. doi: 10.1371/journal.ppat.1003729 24244160

11. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, et al. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science. 2011; 332(6026): 254–256. doi: 10.1126/science.1199410 21474763

12. Xu P, Liu Y, Graham RI, Wilson K, Wu K. Densovirus is a mutualistic symbiont of a global crop pest (Helicoverpa armigera) and protects against a baculovirus and Bt biopesticide. PLoS Pathog. 2014; 10(10): e100449.

13. Jagdale SS, Joshi RS. Facilitator roles of viruses in enhanced insect resistance to biotic stress. Curr Opin Insect Sci. 2019; 33(Jun 2019): 111–116. doi: 10.1016/j.cois.2019.05.008 31358189

14. Zhao T, Ganji S, Schiebe C, Bohman B, Weinstein P, Krokene P, et al. Convergent evolution of semiochemicals across Kingdoms: bark beetles and their fungal symbionts. ISME J. 2019; 13(6): 1535–1545. doi: 10.1038/s41396-019-0370-7 30770902

15. Hunter MS, Asiimwe P, Himler AG, Kelly SE. Host nuclear genotype influences phenotype of a conditional mutualist symbiont. J Evol Biol. 2017; 30(1): 141–149. doi: 10.1111/jeb.12993 27748992

16. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM. Introduced species and their missing parasites. Nature. 2003; 421(6923): 628–630. doi: 10.1038/nature01346 12571595

17. Prenter J, Macneil C, Dick JT, Dunn AM. Roles of parasites in animal invasions. Trends Ecol Evol. 2004; 19(7): 385–390. doi: 10.1016/j.tree.2004.05.002 16701290

18. Girardoz S, Kenis M, Quicke DLJ. Recruitment of native parasitoids by an exotic leaf miner, Cameraria ohridella: host-parasitoid synchronization and influence of the environment. Agr Forest Entomol. 2006; 8(1):49–56.

19. Dunn AM. Parasites and biological invasions. Adv Parasitol. 2009; 68: 161–184. doi: 10.1016/S0065-308X(08)00607-6 19289194

20. Rose DJW, Dewhurst CF, Page WW. The African Armyworm Handbook. 2nd ed. Chatham: Natural Resources Institute; 2000.

21. Grzywacz D, Mushobozi WL, Parnell M, Jolliffe F, Wilson K. Evaluation of Spodoptera exempta nucleopolyhedrovirus (SpexNPV) for the field control of African armyworm (Spodoptera exempta) in Tanzania. Crop Prot. 2008; 27(1): 17–24.

22. Redman EM, Wilson K, Grzywacz D, Cory JS. High levels of genetic diversity in Spodoptera exempta NPV from Tanzania. J Invertebr Pathol. 2010; 105(2): 190–193. doi: 10.1016/j.jip.2010.06.008 20600096

23. Early R. González-Moreno P, Murphy ST, Day R. Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. NeoBiota. 2018; 40(Nov 9): 25–50.

24. Pogue M. A world revision of the genus Spodoptera Guenee (Lepidoptera: Noctuidae). Mem Am Ent Soc. 2002; 43: 1–202.

25. Montezano DG, Specht A, Sosa-Gomez DR, Roque-Specht VF, Sousa-Silva JC, Paula-Moraes SV, et al. (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr Entomol. 2018; 26(2): 286–300.

26. Jing D, Guo J, Jiang Y, Zhao J, Sethi A, He K, et al. Initial detections and spread of invasive Spodoptera frugiperda in China and comparisons with other noctuid larvae in cornfields using molecular techniques. Insect Sci. 2019; doi: 10.1111/1744-7917.12700 31209955

27. Goergen G, Kumar PL, Sankung SB, Togola A, Tamo M. First report of outbreaks of the Fall Armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in west and central Africa. PLoS One. 2016; 11(10): e0165632. doi: 10.1371/journal.pone.0165632 27788251

28. Reichelderfer CF, Benton CV. Some genetic aspects of the resistance of Spodoptera frugiperda to a nuclear polyhedrosis virus. J Invertebr Pathol. 1974; 23(3): 378–382. doi: 10.1016/0022-2011(74)90105-0 4597766

29. Escribano A, Williams T, Goulson D, Cave RD, Chapman JW, Caballero P. Selection of a nucleopolyhedrovirus for control of Spodoptera frugiperda (Lepidoptera: Noctuidae): structural, genetic, and biological comparison of four isolates from the Americas. J Econ Entomol. 1999; 92(5): 1079–1085. doi: 10.1093/jee/92.5.1079 10582046

30. Simon O, Williams T, Lopez-Ferber M, Caballero P. Genetic structure of a Spodoptera frugiperda nucleopolyhedrovirus population: high prevalence of deletion genotypes. Appl Environ Microbiol. 2004; 70(9): 5579–5588. doi: 10.1128/AEM.70.9.5579-5588.2004 15345446

31. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol. 2011; 29(7): 644–652. doi: 10.1038/nbt.1883 21572440

32. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015; 12(1): 59–60. doi: 10.1038/nmeth.3176 25402007

33. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007; 35(Web Server issue): W182–W185. doi: 10.1093/nar/gkm321 17526522

34. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Roble M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21(18): 3674–3676. doi: 10.1093/bioinformatics/bti610 16081474

35. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, et al. InterProScan: protein domains identifier. Nucleic Acids Res. 2005; 33(Web Server issue): W116–W120. doi: 10.1093/nar/gki442 15980438

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

37. Nibert ML, Ghabrial SA, Maiss E, Lesker T, Vainio EJ, Jiang D, et al. Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Res. 2014; 188(Aug 8): 128–141.

38. Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016; 33(7): 1870–1874. doi: 10.1093/molbev/msw054 27004904

39. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009; 25(15): 1972–1973. doi: 10.1093/bioinformatics/btp348 19505945

40. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015; 32(1): 268–274. doi: 10.1093/molbev/msu300 25371430

41. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017; 14(6): 587–589. doi: 10.1038/nmeth.4285 28481363

42. Minh BQ, Nguyen MA, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 2013; 30(5): 1188–1195. doi: 10.1093/molbev/mst024 23418397

43. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC bioinformatics. 2011; 12: 323. doi: 10.1186/1471-2105-12-323 21816040

44. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010; 26(1): 139–140. doi: 10.1093/bioinformatics/btp616 19910308

45. Klopfenstein DV, Zhang L, Pedersen BS, Ramirez F, Warwick Vesztrocy A, Naldi A, et al. GOATOOLS: A Python library for Gene Ontology analyses. Sci rep. 2018; 8(1): 10872. doi: 10.1038/s41598-018-28948-z 30022098

46. R Development Core Team. R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria (ISBN 3-900051-07-0). Retrieved from http://www.R-project.org. 2008.

47. Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 25(7): 1307–1320. doi: 10.1093/molbev/msn067 18367465

48. Loewe L. Negative selection. Nature Education, 2008; 1(1): 59.

49. Simmonds P, Adams MJ, Benko M, Breitbart M, Brister JR, Carstens EB, et al. Consensus statement: Virus taxonomy in the age of metagenomics. Nat Rev Microbiol. 2017; 15(3): 161–168. doi: 10.1038/nrmicro.2016.177 28134265

50. Vainio EJ, Chiba S, Ghabrial SA, Maiss E, Roossinck M, Sabanadzovic S, et al. ICTV Virus Taxonomy Profile: Partitiviridae. J Gen Virol. 2018; 99(1): 17–18. doi: 10.1099/jgv.0.000985 29214972

51. Saridaki A, Bourtzis K. Wolbachia: more than just a bug in insects genitals. Curr Opin Microbiol. 2010; 13(1): 67–72. doi: 10.1016/j.mib.2009.11.005 20036185

52. Longdon B, Jiggins FM. Vertically transmitted viral endosymbionts of insects: do sigma viruses walk alone? Proc Biol Sci. 2012; 279(1744): 3889–3898. doi: 10.1098/rspb.2012.1208 22859592

53. Zhou M, Sun X, Vlak JM, Hu Z, van der Werf W. Horizontal and vertical transmission of wild-type and recombinant Helicoverpa armigera single-nucleocapsid nucleopolyhedrovirus. J Invertebr Pathol. 2005; 89(2): 165–175. doi: 10.1016/j.jip.2005.03.005 15893760

54. Chen Y, Evans J, Feldlaufer M. Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J Invertebr Pathol. 2006; 92(3): 152–159. doi: 10.1016/j.jip.2006.03.010 16793058

55. Mondotte JA, Gausson V, Frangeul L, Blanc H, Lambrechts L, Saleh MC. Immune priming and clearance of orally acquired RNA viruses in Drosophila. Nat Microbiol. 2018; 3(12): 1394–1403. doi: 10.1038/s41564-018-0265-9 30374170

56. Hughes GL, Rasgon JL. Transinfection: a method to investigate Wolbachia-host interactions and control arthropod-borne disease. Insect Mol Biol. 2014; 23(2): 141–151. doi: 10.1111/imb.12066 24329998

57. de Miranda JR, Genersch E. Deformed wing virus. J Invertebr Pathol. 2010; 103(Suppl 1): S48–61.

58. Strand MR, Burke GR. Polydnaviruses: Nature's Genetic Engineers. Annu Rev Virol. 2014; 1: 333–354. doi: 10.1146/annurev-virology-031413-085451 26958725

59. Jiu M, Zhou X, Tong L, Xu J, Yang X, Wan F, et al. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS One. 2007; 2(1): e182. doi: 10.1371/journal.pone.0000182 17264884

60. Thomas-Orillard M. A virus–Drosophila association: the first steps towards co-evolution? Biodivers Conserv. 1996; 5(8): 1015–1021.

61. Dheilly NM. Holobiont-Holobiont interactions: redefining host-parasite interactions. PLoS Pathog. 2014; 10(7): e1004093. doi: 10.1371/journal.ppat.1004093 24992663

62. Liu J. SARS, wildlife, and human health. Science. 2003; 302(5642): 53.

63. Lai S, Qin Y, Cowling BJ, Ren X, Wardrop NA, Gilbert M, et al. Global epidemiology of avian influenza A H5N1 virus infection in humans, 1997–2015: a systematic review of individual case data. Lancet Infect Dis. 2016; 16(7): e108–e118.

64. Yiu Lai K, Wing Yiu Ng G, Fai Wong K, Fan Ngai Hung I, Kam Fai Hong J, Fan Cheng F, et al. Human H7N9 avian influenza virus infection: a review and pandemic risk assessment. Emerg Microbes Infect. 2013; 2(8): e48. doi: 10.1038/emi.2013.48 26038484

65. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature. 2011; 476(7361): 454–457. doi: 10.1038/nature10356 21866160

66. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell. 2009; 139(7): 1268–1278. doi: 10.1016/j.cell.2009.11.042 20064373

67. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, et al. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature. 2011; 476(7361): 450–453. doi: 10.1038/nature10355 21866159

68. Bull J. Evolution of sex determining mechanisms. Menlo Park (California): Benjamin Cummings Publishing; 1983.

69. Hurst GD, Frost CL. Reproductive parasitism: maternally inherited symbionts in a biparental world. Cold Spring Harb Perspect Biol. 2015; 7(5): a017699. doi: 10.1101/cshperspect.a017699 25934011

70. Graham RI, Wilson K. Male-killing Wolbachia and mitochondrial selective sweep in a migratory African insect. BMC Evol Biol. 2012; 12(204): 204.

71. Duneau DF, Kondolf HC, Im JH, Ortiz GA, Chow C, Fox MA, et al. The Toll pathway underlies host sexual dimorphism in resistance to both Gram-negative and Gram-positive bacteria in mated Drosophila. BMC Biol. 2017; 15(1): 124. doi: 10.1186/s12915-017-0466-3 29268741

72. Park SJ, Kim YI, Park A, Kwon HI, Kim EH, Si YJ, et al. Ferret animal model of severe fever with thrombocytopenia syndrome phlebovirus for human lethal infection and pathogenesis. Nat Microbiol. 2018; 4(3): 438–446. doi: 10.1038/s41564-018-0317-1 30531978

73. Jindra M, Palli SR, Riddiford LM. The juvenile hormone signaling pathway in insect development. Annu Rev Entomol. 2013; 58: 181–204. doi: 10.1146/annurev-ento-120811-153700 22994547

74. Kingsolver MB, Hardy RW. Making connections in insect innate immunity. Proc Natl Acad Sci U S A. 2012; 109(46): 18639–18640. doi: 10.1073/pnas.1216736109 23100537

75. Kingsolver MB, Huang Z, Hardy RW. Insect antiviral innate immunity: pathways, effectors, and connections. J Mol Biol. 2013; 425(24): 4921–4936. doi: 10.1016/j.jmb.2013.10.006 24120681

76. Lin X, Smagghe G. Roles of the insulin signaling pathway in insect development and organ growth. Peptides. 2018; 258(SI): 149–156.

77. Shields VDC editor. Insect Physiology and Ecology. In Rosales Ceditor. Cellular and Molecular Mechanisms of Insect Immunity. London: IntechOpen; 2017. p. 179–212.

78. Roy S, Saha TT, Zou Z, Raikhel AS. Regulatory pathways controlling female insect reproduction. Annu Rev Entomol. 2018; 63: 489–511. doi: 10.1146/annurev-ento-020117-043258 29058980

79. Marques JT, Imler JL. The diversity of insect antiviral immunity: insights from viruses. Curr Opin Microbiol. 2016; 32: 71–76. doi: 10.1016/j.mib.2016.05.002 27232381

80. Cheng T, Lin P, Huang L, Wu Y, Jin S, Liu C, et al. Genome-wide analysis of host responses to four different types of microorganisms in Bombyx mori (Lepidoptera: Bombycidae). J Insect Sci. 2016; 69(1): 1–11.

81. Nguyen Q, Palfreyman RW, Chan LC, Reid S, Nielsen LK. Transcriptome sequencing of and microarray development for a Helicoverpa zea cell line to investigate in vitro insect cell-baculovirus interactions. PLoS One. 2012; 7(5): e36324. doi: 10.1371/journal.pone.0036324 22629315

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