Transcriptome-Based Analysis of the Mechanism of Acute Manganese-Induced Immune Function Decline and Metabolic Disorders in Estuarine Tapertail Anchovy (Coilia nasus)

To characterize the transcriptional and physiological alterations induced by manganese stress in Coilia nasus, juveniles (mean weight 5.0 ± 0.2 g) were subjected to either manganese exposure (5.50 ± 0.03 mg/L) or control (0 mg/L) for a 12 h period. Subsequently, gill tissues were excised for evaluation of antioxidant parameters and RNA-Seq analysis. A total of 753 DEGs were identified in the manganese exposure group compared to controls, comprising 287 up-regulated and 466 down-regulated genes. GO and KEGG enrichment analysis of DEGs showed that most of the DEGs were involved in immune and metabolic pathways, which disturbed the biological processes related to immunity and metabolism at the molecular level. The acute manganese stress initiated a multi-level antioxidant response to cope with oxidative stress in Coilia nasus. This finding was further supported by the significant increase in MDA content and significant decrease in GSH content and GSH-Px activity under manganese exposure, while SOD and CAT activities were significantly increased. Simultaneously, the acute manganese stress triggered profound metabolic reprogramming to cope with energy pressure in Coilia nasus, which showed that manganese exposure significantly down-regulated energy metabolism-related genes (pfkm, pgam2, eno3, pkm, aqp9, apoa1, tkt, sds); furthermore, the overall energy metabolism network was widely inhibited, while lipid metabolism-related genes (fabp3, cpt1a) were significantly up-regulated to compensatorily activate fatty acid transport and β-oxidation pathways. In addition, the acute manganese stress initiated a complex immune response pattern to cope with cell damage in Coilia nasus, which showed that manganese exposure significantly enhanced the expression of inflammatory signaling genes (mapk1, stat1, tgfb3); furthermore, certain inflammatory pathways were activated, while the expressions of immune regulatory genes (traf6, il-10) were significantly decreased. In summary, these results indicated that manganese exposure could impair immune function, disrupt metabolism, and induce oxidative stress in Coilia nasus.