The multi-omics approach reveals the impact of Temnocephala digitata infection on Macrobrachium rosenbergii

Abstract

Macrobrachium rosenbergii (M. rosenbergii) is a vital freshwater economic species, and no prior reports exist on its infection by the symbiotic flatworm Temnocephala digitata (Platyhelminthes: Temnocephalidae; T. digitata). However, during aquaculture practices, we observed that T. digitata infection caused growth retardation and even mortality in M. rosenbergii. This study investigates the pathogenic mechanisms of T. digitata infection in M. rosenbergii using a multi-omics approach. Results revealed that T. digitata infection induced growth retardation, immune suppression, and metabolic dysregulation in the shrimp. Intestinal microbiota analysis demonstrated microbial dysbiosis characterized by an increased abundance of Proteobacteria (particularly the opportunistic pathogenic genus Aeromonas) and reduced proportions of Firmicutes and Bacteroidota. Integrated transcriptomic and metabolomic analyses showed that T. digitata infection suppressed ribosomal functions, lipid metabolism, and protein metabolism in gill tissues while concurrently activating inflammatory factors and pathways (e.g., TNF-α, COX-2, and Toll/IMD signaling). Additionally, infection induced abnormal molting behavior by upregulating ecdysone (ECD), and methyl farnesoate (MF) while suppressing molt-inhibiting hormone (MIH), exacerbating energy depletion and immune exhaustion. Multi-omics correlation analysis further elucidated complex interactions among core gut microbiota, key metabolites, and hub genes, collectively driving nutrient-immune imbalance. Histopathological examinations confirmed hepatopancreatic vacuolization, intestinal villi atrophy, and gill lesions, consistent with metabolic and immune dysfunction. This study provides the first evidence of T. digitata-associated pathogenicity in M. rosenbergii, revealing that the symbiont-host interaction disrupts nutrient metabolism-immune homeostasis, thereby precipitating a health crisis. These findings advance understanding of temnocephalid-crustacean relationships and highlight risks of symbiont overproliferation in aquaculture systems.