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

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.

Characterization of the mitochondrial genome of Spodoptera exempta (Lepidoptera: Noctuidae) from South Africa

“…exempta results in the initiation of larval outbreaks, which can cause severe damage to rangeland grasses and crops, including maize, millet, rice, wheat, among others (Parker and Gatehouse 1985a , 1985b ; Xu et al. 2020 ). To date, S .…”

The Effect of Phenoloxidase Activity on Survival Is Host Plant Dependent in Virus-Infected Caterpillars

“…For individuals reared on L. albifrons , survival was enhanced when infected with the virus, regardless of immunocompetence as measured by PO. This curious result requires further investigation, but it is noteworthy that at least one other study found higher survival frequency in individuals infected with a densovirus ( Xu et al 2014 ), indicating that under certain conditions not all viruses are pathogenic ( Suttle 2013 , Roossinck 2015 , Xu et al 2020 ). We suggest that future studies delve into differences in host plant traits that may contribute to different outcomes of pathogen infection.…”

Structure of a Plant-Specific Partitivirus Capsid Reveals a Novel Coat Protein Architecture with a Hypervariable Protrusion

“…Given the apparent lack of horizontal transmission of partitiviruses, it is not clear how deltapartitiviruses found their plant hosts, although there is a close relationship between plant and fungal partitiviruses (Roossinck, 2019). In addition to infecting plants, fungi and protozoa, partitivirus-like sequences have now been found to be common in wild populations of arthropods (Pettersson et al, 2019) where they are also vertically transmitted (Cross et al, 2020;Xu et al, 2020).…”