Symbiotic bracovirus of a parasite manipulates host lipid metabolism via tachykinin signaling

Parasites alter host energy homeostasis for their own development, but the mechanisms underlying this phenomenon remain largely unknown. Here, we show that Cotesia vestalis, an endoparasitic wasp of Plutella xylostella larvae, stimulates a reduction of host lipid levels. This process requires excess secretion of P. xylostella tachykinin (PxTK) peptides from enteroendocrine cells (EEs) in the midgut of the parasitized host larvae. We found that parasitization upregulates PxTK signaling to suppress lipogenesis in midgut enterocytes (ECs) in a non-cell-autonomous manner, and the reduced host lipid level benefits the development of wasp offspring and their subsequent parasitic ability. We further found that a C. vestalis bracovirus (CvBV) gene, CvBV 9-2, is responsible for PxTK induction, which in turn reduces the systemic lipid level of the host. Taken together, these findings illustrate a novel mechanism for parasite manipulation of host energy homeostasis by a symbiotic bracovirus gene to promote the development and increase the parasitic efficiency of an agriculturally important wasp species. Author summary Parasitic wasps are ubiquitous on earth and diverse. They lay eggs in or on the bodies of their hosts, and they have evolved adaptive strategies to regulate the energy metabolism of their hosts to match their own specific nutrition requirements. Here, we found that Cotesia vestalis, a solitary endoparasitoid of Plutella xylostella, uses symbiotic bracovirus as a weapon to manipulate host systemic lipid levels. Specifically, a C. vestalis bracovirus (CvBV) gene, CvBV 9-2, is responsible for the induction of PxTK, which in turn suppresses lipogenesis in the midgut of the parasitized host, leading to a nutritional lipid level suitable for the development and subsequent parasitic efficiency of C. vestalis wasps. Our study provides innovative insights into the mechanisms by which parasitic wasps manipulate host lipid homeostasis and may help to expand our knowledge of other parasitic systems.

Automated summary

Parasitoid wasps, such as Cotesia vestalis, manipulate host energy homeostasis by using symbiotic bracovirus genes to promote their own development and increase parasitic efficiency.