A dipteran parasite regulates 20E synthesis and antibacterial activity of the host for development through inducing host nitric oxide production

Abstract

Parasites primarily rely on the host to survive, and have evolved diverse survival strategies. In the present study, we report a specific survival strategy of a dipteran parasite Exorista sorbillans (Diptera: Tachinidae), which is a potential biological control agent for agricultural pests and a pest in sericulture. We found that the expression levels of host nitric oxide synthase (NOS) and nitric oxide (NO) production were increased after E. sorbillans infection. Reducing NOS expression and NO production with a NOS inhibitor (L-NAME) in infected hosts significantly impeded the growth of E. sorbillans larvae. Moreover, the 20-hydroxyecdysone (20E) biosynthesis of infected hosts was elevated with increasing NO production, and inhibiting NOS expression also lowered 20E biosynthesis. More importantly, induced NO synthesis was required to eliminate intracellular bacterial pathogens that presumably competed for shared host resources. Inhibiting NOS expression down-regulated the transcription of antimicrobial peptide genes and increased the number of bacteria in infected hosts. Collectively, this study revealed a new perspective on the role of NO in host-parasite interactions and a novel mechanism for parasite regulation of host to support its development. Author summaryParasites are ubiquitous on earth and diverse, and have evolved various strategies to match their own specific requirements for survival within the host. In this study, we found that Exorista sorbillans, an endoparasite of many agricultural pests and the main insect pest in sericulture, used a novel strategy to manipulate its host NO synthesis for survival within its host Bombyx mori. Specifically, NOS expression and the production of NO in the host were up-regulated by E. sorbillans infection, which benefited larval E. sorbillans development. Meanwhile, increased NO production in host activated 20E synthesis of parasitized hosts and triggered the expression of AMPs against the invasion of pathogenic bacteria to avoid nutritional competence in the host. Our study provides innovative insights into the mechanisms by which a parasite manipulates host NO production for development and may help to expand our knowledge of other parasitic systems.