White spot syndrome virus (WSSV) modulates lipid metabolism in white shrimp

Abstract In addition to the Warburg effect, which increases the availability of energy and biosynthetic building blocks in WSSV-infected shrimp, WSSV also induces both lipolysis at the viral genome replication stage (12 hpi) to provide material and energy for the virus replication, and lipogenesis a...

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Main Authors: Yen Siong Ng, Cheng-Shun Cheng, Masahiro Ando, Yi-Ting Tseng, Shu-Ting He, Chun-Yuan Li, Shu-Wen Cheng, Yi-Min Chen, Ramya Kumar, Chun-Hung Liu, Haruko Takeyama, Ikuo Hirono, Han-Ching Wang
Format: Article
Language:English
Published: Nature Portfolio 2023-05-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-023-04924-w
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author Yen Siong Ng
Cheng-Shun Cheng
Masahiro Ando
Yi-Ting Tseng
Shu-Ting He
Chun-Yuan Li
Shu-Wen Cheng
Yi-Min Chen
Ramya Kumar
Chun-Hung Liu
Haruko Takeyama
Ikuo Hirono
Han-Ching Wang
author_facet Yen Siong Ng
Cheng-Shun Cheng
Masahiro Ando
Yi-Ting Tseng
Shu-Ting He
Chun-Yuan Li
Shu-Wen Cheng
Yi-Min Chen
Ramya Kumar
Chun-Hung Liu
Haruko Takeyama
Ikuo Hirono
Han-Ching Wang
author_sort Yen Siong Ng
collection DOAJ
description Abstract In addition to the Warburg effect, which increases the availability of energy and biosynthetic building blocks in WSSV-infected shrimp, WSSV also induces both lipolysis at the viral genome replication stage (12 hpi) to provide material and energy for the virus replication, and lipogenesis at the viral late stage (24 hpi) to complete virus morphogenesis by supplying particular species of long-chain fatty acids (LCFAs). Here, we further show that WSSV causes a reduction in lipid droplets (LDs) in hemocytes at the viral genome replication stage, and an increase in LDs in the nuclei of WSSV-infected hemocytes at the viral late stage. In the hepatopancreas, lipolysis is triggered by WSSV infection, and this leads to fatty acids being released into the hemolymph. β-oxidation inhibition experiment reveals that the fatty acids generated by WSSV-induced lipolysis can be diverted into β-oxidation for energy production. At the viral late stage, WSSV infection leads to lipogenesis in both the stomach and hepatopancreas, suggesting that fatty acids are in high demand at this stage for virion morphogenesis. Our results demonstrate that WSSV modulates lipid metabolism specifically at different stages to facilitate its replication.
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spelling doaj.art-f34decb3343547c08d48fd0a808663562023-05-21T11:23:42ZengNature PortfolioCommunications Biology2399-36422023-05-016111110.1038/s42003-023-04924-wWhite spot syndrome virus (WSSV) modulates lipid metabolism in white shrimpYen Siong Ng0Cheng-Shun Cheng1Masahiro Ando2Yi-Ting Tseng3Shu-Ting He4Chun-Yuan Li5Shu-Wen Cheng6Yi-Min Chen7Ramya Kumar8Chun-Hung Liu9Haruko Takeyama10Ikuo Hirono11Han-Ching Wang12Department of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung UniversityDepartment of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung UniversityResearch Organization for Nano and Life Innovations, Waseda UniversityDepartment of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung UniversityDepartment of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung UniversityDepartment of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung UniversityDepartment of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung UniversityDepartment of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung UniversityDepartment of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung UniversityDepartment of Aquaculture, National Pingtung University of Science and TechnologyResearch Organization for Nano and Life Innovations, Waseda UniversityDepartment of Marine Biosciences, Tokyo University of Marine Science and TechnologyDepartment of Biotechnology and Bioindustry Sciences, College of Bioscience and Biotechnology, National Cheng Kung UniversityAbstract In addition to the Warburg effect, which increases the availability of energy and biosynthetic building blocks in WSSV-infected shrimp, WSSV also induces both lipolysis at the viral genome replication stage (12 hpi) to provide material and energy for the virus replication, and lipogenesis at the viral late stage (24 hpi) to complete virus morphogenesis by supplying particular species of long-chain fatty acids (LCFAs). Here, we further show that WSSV causes a reduction in lipid droplets (LDs) in hemocytes at the viral genome replication stage, and an increase in LDs in the nuclei of WSSV-infected hemocytes at the viral late stage. In the hepatopancreas, lipolysis is triggered by WSSV infection, and this leads to fatty acids being released into the hemolymph. β-oxidation inhibition experiment reveals that the fatty acids generated by WSSV-induced lipolysis can be diverted into β-oxidation for energy production. At the viral late stage, WSSV infection leads to lipogenesis in both the stomach and hepatopancreas, suggesting that fatty acids are in high demand at this stage for virion morphogenesis. Our results demonstrate that WSSV modulates lipid metabolism specifically at different stages to facilitate its replication.https://doi.org/10.1038/s42003-023-04924-w
spellingShingle Yen Siong Ng
Cheng-Shun Cheng
Masahiro Ando
Yi-Ting Tseng
Shu-Ting He
Chun-Yuan Li
Shu-Wen Cheng
Yi-Min Chen
Ramya Kumar
Chun-Hung Liu
Haruko Takeyama
Ikuo Hirono
Han-Ching Wang
White spot syndrome virus (WSSV) modulates lipid metabolism in white shrimp
Communications Biology
title White spot syndrome virus (WSSV) modulates lipid metabolism in white shrimp
title_full White spot syndrome virus (WSSV) modulates lipid metabolism in white shrimp
title_fullStr White spot syndrome virus (WSSV) modulates lipid metabolism in white shrimp
title_full_unstemmed White spot syndrome virus (WSSV) modulates lipid metabolism in white shrimp
title_short White spot syndrome virus (WSSV) modulates lipid metabolism in white shrimp
title_sort white spot syndrome virus wssv modulates lipid metabolism in white shrimp
url https://doi.org/10.1038/s42003-023-04924-w
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