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

Pengjun Xu,Kenneth Wilson,Kongming Wu,Xianming Yang,Tong Li,Robert I Graham,Liyu Yang,Darren J Obbard

doi:10.1371/journal.ppat.1008467

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.

Highlights

The development of generation sequencing (NGS) technologies has facilitated the discovery and analysis of novel pathogens with or without overt symptoms, e.g. thousands of viruses have been reported in vertebrate and invertebrate species using metagenomic and transcriptomic sequencing technologies [1,2,3,4,5]
Can we find new pathogens for pest management by determining the interactions between these symbionts and their hosts? Second, how do these newly-discovered symbionts interact with known pathogens, including biopesticides? And third, how do these symbionts behave in novel hosts to which they have not co-evolved? This latter question is pertinent to newly-introduced invasive host species, which may have fewer parasites in the new range than in their native range [16], but may become exposed to novel parasites from other host species in their new environment [17,18,19]
The transcriptional profiles of infected and non-infected individuals were consistent with the phenotypes of these two species having different gene expression profiles in response to infection by partiti-like viruses. These results suggest that the partiti-like viruses are conditional mutualistic symbionts in S. exempta, protecting it when challenged with baculovirus, but are parasitic in its novel host, S. frugiperda

Summary

Introduction

The development of generation sequencing (NGS) technologies has facilitated the discovery and analysis of novel pathogens with or without overt symptoms, e.g. thousands of viruses have been reported in vertebrate and invertebrate species using metagenomic and transcriptomic sequencing technologies [1,2,3,4,5]. Insect pathogens (including bacteria, fungi and viruses) that naturally kill their hosts can be harnessed as potential biopesticides [6,7,8]. Co-infection of symbionts may alter the levels of resistance of their hosts to other pathogens, including those used in biopesticides (e.g. baculoviruses) [9,12]. The identification of novel symbionts using NGS raises a number of questions. Can we find new pathogens for pest management by determining the interactions between these symbionts and their hosts? How do these newly-discovered symbionts interact with known pathogens, including biopesticides (e.g. baculoviruses)? Can we find new pathogens for pest management by determining the interactions between these symbionts and their hosts? Second, how do these newly-discovered symbionts interact with known pathogens, including biopesticides (e.g. baculoviruses)? And third, how do these symbionts behave in novel hosts to which they have not co-evolved? This latter question is pertinent to newly-introduced invasive host species, which may have fewer parasites in the new range than in their native range [16], but may become exposed to novel parasites from other host species in their new environment [17,18,19]

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Discussion

Conclusion