The influence of Enterocytozoon hepatopenaei infection on lipid and immune pathways in Litopenaeus vannamei

Abstract

Hepatopancreatic microsporidiosis (HPM) caused by Enterocytozoon hepatopenaei (EHP) is a devastating disease in shrimp aquaculture, characterized by severe growth retardation. To characterize hepatopancreatic molecular responses associated with EHP challenge, we performed an integrated transcriptomic and metabolomic analysis of Litopenaeus vannamei following oral challenge. EHP infection was confirmed by PCR. Transcriptomic profiling identified 5490 differentially expressed genes (DEGs), with notable suppression of ribosomal pathway genes, suggesting a potential constraint on host biosynthetic capacity. Conversely, genes involved in lipid metabolism (e.g., PNLIP, GPAT3, ACOX1) were significantly upregulated. Immune signaling-related genes showed mixed regulation, including upregulation of JAK2 and PLCG1 and downregulation of PIK3CA and PLCB. Metabolomic analysis revealed significant lipid alterations (42.5% of differential metabolites). Phosphatidylserine (PS) was significantly upregulated, while linoleic acid, CDP-diacylglycerol (CDP-DAG), phosphatidylglycerol phosphate (PGP), phosphatidylethanolamine (PE) species, 9,10-DiHOME, and 4 diacylglycerol (DG) were significantly downregulated. Integrated multi-omics analysis highlighted the glycosylphosphatidylinositol (GPI)-anchor biosynthesis pathway as a prominent co-enriched pathway. The discordance between downregulated upstream genes (PIG-A, PIG-L) and altered downstream phosphatidylethanolamine (PE) abundance indicates remodeling of host membrane-related metabolism, although direct parasite-driven resource appropriation remains to be demonstrated. These findings reveal coordinated alterations in ribosome-related transcription, lipid metabolism, and immune-associated pathways in the EHP-challenged group at 14 days post-challenge, providing candidate mechanisms for further functional validation.