Lipidomic Profiling Reveals Distinct Differences in Sphingolipids Metabolic Pathway between Healthy Apis cerana cerana larvae and Chinese Sacbrood Disease

SIMPLE SUMMARY: Chinese Sacbrood Virus (CSBV) is one of the most destructive viruses; it causes Chinese sacbrood disease (CSD) in Apis cerana cerana, resulting in heavy economic loss. In this study, the first comprehensive analysis of the lipidome of A. c. cerana larvae-infected CSBV was performed. Viruses rely on host metabolites to infect, replicate and disseminate from several tissues. The metabolic environments play crucial roles in these processes amplification and reproduction processes. Using high-resolution mass spectrometry, we profiled 2164 lipids in larva samples obtained from healthy controls and larvae with CSBV infection. A total of 266 lipids, including categories of DG, TG, PC, PE, SM and Cer, were significantly changed after CSBV infection, considering that qRT-PCR showed that seven sphingolipid enzymes involved in the sphingolipid pathway were increased. This suggests that the lipidome of honeybee larvae is altered in CSBV infection, and sphingolipids may contribute to CSD progression. Specific changes in the lipidome such as TG (39:6), which showed a more than 10-fold increase, may be possible targets for the detection of CSD. Lipid pathways analyses revealed that glycerophospholipid metabolism was the most enriched pathway and may be associated with CSBV infection. ABSTRACT: Chinese sacbrood disease (CSD), which is caused by Chinese sacbrood virus (CSBV), is a major viral disease in Apis cerana cerana larvae. Analysis of lipid composition is critical to the study of CSBV replication. The host lipidome profiling during CSBV infection has not been conducted. This paper identified the lipidome of the CSBV–larvae interaction through high-resolution mass spectrometry. A total of 2164 lipids were detected and divided into 20 categories. Comparison of lipidome between healthy and CSBV infected-larvae showed that 266 lipid species were altered by CSBV infection. Furthermore, qRT-PCR showed that various sphingolipid enzymes and the contents of sphingolipids in the larvae were increased, indicating that sphingolipids may be important for CSBV infection. Importantly, Cer (d14:1 + hO/21:0 + O), DG (41:0e), PE (18:0e/18:3), SM (d20:0/19:1), SM (d37:1), TG (16:0/18:1/18:3), TG (18:1/20:4/21:0) and TG (43:7) were significantly altered in both CSBV_24 h vs. CK_24 h and CSBV_48 h vs. CK_48 h. Moreover, TG (39:6), which was increased by more than 10-fold, could be used as a biomarker for the early detection of CSD. This study provides evidence that global lipidome homeostasis in A. c. cerana larvae is remodeled after CSBV infection. Detailed studies in the future may improve the understanding of the relationship between the sphingolipid pathway and CSBV replication.