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

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. Author summary Modern molecular approaches allow the discovery of new viruses that do not present obvious symptoms of disease in their hosts. Using these methods, we discovered three new partiti-like viruses in a major crop pest, the African armyworm, Spodoptera exempta, which are naturally transmitted vertically from adult females to their offspring in her eggs. We discovered that these viruses decrease their host's growth rate and reproduction, but they may also help their insect host by protecting them from other lethal viruses, specifically the baculoviruses that are often used as biological pesticides. We transferred these partiti-like viruses into a novel host, the Fall armyworm, S. frugiperda, by microinjection and found that they also decrease S. frugiperda's growth rate and reproduction. Interestingly, however, it appears that the partiti-like viruses make S. frugiperda more susceptible to baculovirus, potentially making it more vulnerable to control using biopesticides. Our results suggest a possible novel pest management strategy via artificial host-shift of viruses discovered using molecular approaches and offers new insights into host-virus-virus interactions.