Multi-omics profiling reveals the molecular mechanisms of H2O2-induced detrimental effects on Thamnaconus septentrionalis.

Background: Hydrogen peroxide (H₂O₂), a novel water treatment agent, can be used for disinfection, water quality adjustment, and disease prevention, while excessive H₂O₂ can injure farm animals, even leading to death. Hydrogen peroxide is a recommended disinfectant and bactericide for treating gill diseases and vibriosis in the greenfin horse-faced filefish Thamnaconus septentrionalis. However, its cumulative effect, toxic molecular mechanism and relevant signal transduction/metabolic networks in marine fishes are largely unknown.

Results: We employed a multi-omics approach to investigate the detrimental effects of 50 mg/L H₂O₂ exposure (2 h/d) on filefish for 2 d, 4 d, and 6 d. Transcriptome sequencing showed that differentially expressed genes (DEGs) were mainly classified into functions such as signal transduction, nervous system, liver and bile acid metabolism, energy metabolism, cell adhesion and communication, inflammation and immune response. Metabolomic analysis found that the significantly changed metabolites (SCMs) were involved in phenylalanine metabolism, inflammatory mediator regulation, linoleic acid metabolism, and necroptosis. The main SCMs were cholic acid, carnitine C12:1, dimethylmalonic acid, glutamic acid, L-lactic acid, shikimic acid, 2-methylsuccinic acid, and others. Moreover, H₂O₂-induced oxidative stress also disturbs the balance of the gut microbiota, altering the microbial composition and affecting digestive processes.

Conclusions: Integrated multiomics analysis revealed that H₂O₂-induced detrimental impacts include mucosal damage, inflammatory and immune responses, altered energy metabolism, and gut microbiota disorders. These findings offer novel insights into the harmful effects and signal transduction/metabolic pathways triggered by H₂O₂ exposure in marine fishes.