Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana).

Fan Ying,Yue Hao,Yulong Guo,Kai Li,Jie Wu,Huipeng Yang,Hira Mannan,Zhengyi Zhang,Yanping Chen,Mingsheng Zhuang,Liuhao Wang,Jiaxing Huang,Jun Yao,Jilian Li

doi:10.3389/fmicb.2021.615893

Abstract

The honey bee is one of the most important pollinators in the agricultural system and is responsible for pollinating a third of all food we eat. Sacbrood virus (SBV) is a member of the virus family Iflaviridae and affects honey bee larvae and causes particularly devastating disease in the Asian honey bees, Apis cerana. Chinese Sacbrood virus (CSBV) is a geographic strain of SBV identified in China and has resulted in mass death of honey bees in China in recent years. However, the molecular mechanism underlying SBV infection in the Asian honey bee has remained unelucidated. In this present study, we employed high throughput next-generation sequencing technology to study the host transcriptional responses to CSBV infection in A. cerana larvae, and were able to identify genome-wide differentially expressed genes associated with the viral infection. Our study identified 2,534 differentially expressed genes (DEGs) involved in host innate immunity including Toll and immune deficiency (IMD) pathways, RNA interference (RNAi) pathway, endocytosis, etc. Notably, the expression of genes encoding antimicrobial peptides (abaecin, apidaecin, hymenoptaecin, and defensin) and core components of RNAi such as Dicer-like and Ago2 were found to be significantly upregulated in CSBV infected larvae. Most importantly, the expression of Sirtuin target genes, a family of signaling proteins involved in metabolic regulation, apoptosis, and intracellular signaling was found to be changed, providing the first evidence of the involvement of Sirtuin signaling pathway in insects’ immune response to a virus infection. The results obtained from this study provide novel insights into the molecular mechanism and immune responses involved in CSBV infection, which in turn will contribute to the development of diagnostics and treatment for the diseases in honey bees.

Highlights

The Asian honey bee Apis cerana is one of two honey bee species that have been truly domesticated and used in apiculture
Infected larvae fail to pupate while ecdysial fluid rich in Sacbrood virus (SBV) accumulates beneath the unshed larval cuticle, forming the sac, the name “Sacbrood.” Sacbrood disease was first described in the western honey bee A. mellifera in 1913 and later in A. cerana in 1972 (Chen et al, 2017)
The association of Chinese Sacbrood virus (CSBV) with high mortality of Asian honey bee colonies has led to an increased awareness of the risks of viral infections on bee health

Summary

Introduction

The Asian honey bee Apis cerana is one of two honey bee species that have been truly domesticated and used in apiculture. It has adapted diverse environments, and its natural distribution is broad, and is widely distributed in complex topographic regions with different habitats, diverse flora, and divergent climate in Asia (Hepburn and Radloff, 2011). Infected larvae fail to pupate while ecdysial fluid rich in SBV accumulates beneath the unshed larval cuticle, forming the sac, the name “Sacbrood.” Sacbrood disease was first described in the western honey bee A. mellifera in 1913 and later in A. cerana in 1972 (Chen et al, 2017). The severe losses of A. cerana populations across Asia due to SBV disease were caused by a variety of strains of SBV reflecting their geographic isolations, namely Thai Sacbrood virus, Chinese Sacbrood virus, Korean Sacbrood virus, etc. (Bailey et al, 1982; Choe et al, 2012)

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Results

Conclusion