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

Yanping Wang,Min Shi,Sicong Zhou,Ting Chen,Jianhua Huang,Jiani Chen,Zehua Wang,Lan Pang,Xiaotong Wu,Xuexin Chen,Xiqian Ye,Erik H Poelman

doi:10.1371/journal.ppat.1009365

Yanping Wang, Min Shi + Show 10 more

Open Access

https://doi.org/10.1371/journal.ppat.1009365

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Abstract

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.

Highlights

Parasitism is common in nature, and all living organisms are vulnerable to parasites [1]
We found that Cotesia vestalis, a solitary endoparasitoid of Plutella xylostella, uses symbiotic bracovirus as a weapon to manipulate host systemic lipid levels
A C. vestalis bracovirus (CvBV) gene, CvBV 9–2, is responsible for the induction of P. xylostella tachykinin (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

Summary

Introduction

Parasitism is common in nature, and all living organisms are vulnerable to parasites [1]. Parasites depend on their hosts, which provide them with nutrition and habitat, for their development [2,3,4,5,6]. Parasitic factors have been reported to modify host energy metabolism, which in turn provides the parasite with needed nutrients and leads to successful parasitism [19,20,21,22,23]

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