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. 2020 Jun 22;16(6):e1008467. doi: 10.1371/journal.ppat.1008467. eCollection 2020 Jun.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Nucleopolyhedroviruses* / genetics
  • Nucleopolyhedroviruses* / metabolism
  • Phylogeny*
  • Spodoptera / genetics
  • Spodoptera / virology*

Grants and funding

P.X. was funded by a Newton International Fellowship (NF161146) https://royalsociety.org/grants-schemes-awards/grants/newton-international/, the Agricultural Science and Technology Innovation Program (ASTIP-TRIC04 and CAAS-ZDRW202007) http://www.caas.cn/en/research/research_program/index.html, and the Central Public-interest Scientific Institution Basal Research Fund (Y2019YJ06). K.W. and R.I.G. were funded by a Global Challenges Research Fund grant (BB/P023444/1) https://www.ukri.org/research/global-challenges-research-fund/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.