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

Yanping Wang; Xiaotong Wu; Zehua Wang; Ting Chen; Sicong Zhou; Jiani Chen; Lan Pang; Xiqian Ye; Min Shi; Jianhua Huang; Xuexin Chen

doi:10.1371/journal.ppat.1009365

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

PLoS Pathog. 2021 Mar 1;17(3):e1009365. doi: 10.1371/journal.ppat.1009365. eCollection 2021 Mar.

Authors

Yanping Wang^{1

2

3}, Xiaotong Wu^{1

2

3}, Zehua Wang^{1

2

3}, Ting Chen^{1

2

3}, Sicong Zhou^{1

2

3}, Jiani Chen^{1

2

3}, Lan Pang^{1

2

3}, Xiqian Ye^{1

2

3}, Min Shi^{1

2

3}, Jianhua Huang^{1

2

3}, Xuexin Chen^{1

2

3

4}

Affiliations

¹ Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China.
² Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, Zhejiang University, Hangzhou, China.
³ Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Zhejiang University, Hangzhou, China.
⁴ State Key Lab of Rice Biology, Zhejiang University, Hangzhou, China.

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.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Digestive System / metabolism
Host-Parasite Interactions / genetics
Host-Parasite Interactions / immunology*
Larva / metabolism
Larva / virology
Lipid Metabolism / immunology
Lipid Metabolism / physiology*
Parasites / pathogenicity
Parasites / virology*
Polydnaviridae / genetics*
Polydnaviridae / pathogenicity
Signal Transduction / immunology
Signal Transduction / physiology
Wasps / physiology
Wasps / virology

Grants and funding

This work was jointly supported by the Key Program of National Natural Science Foundation of China (31630060), National Key Research and Development Program of China (2019YFD0300104), and the Chinese National Key Project for Basic Research (2013CB127600) to X.C.; the National Key Research and Development Program of China (2017YFD0200400), the National Science Fund for Excellent Young Scholars (31622048), the National Science Foundation of China (31772522), and Zhejiang Provincial Natural Science Foundation of China (LR18C140001) to J.H.; the National Science Foundation of China (31672079) to M.S. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.