Arachidonic Acid Metabolic Rewiring Drives Differential Plant Protein Adaptation in Golden Pompano (Trachinotus ovatus)

The replacement of fishmeal with plant protein is widely regarded as a key strategy for sustainable aquaculture. However, carnivorous marine fish often show limited tolerance to fishmeal-free diets. Here, we investigated growth performance, hepatic physiological responses, and molecular mechanisms underlying adaptation to a soy protein concentrate-based diet (SPCD) in golden pompano (Trachinotus ovatus). An 8-week feeding trial was conducted under communal rearing conditions, followed by the phenotypic stratification of SPCD-fed fish into high- and low-growth subgroups. Growth performance, serum biochemical indices, and liver histology were assessed, and integrated transcriptomic and metabolomic analyses were performed on liver tissue. At the population level, the SPCD resulted in reduced growth, a lower feed intake, and decreased feed utilization efficiency compared with a fishmeal-based diet. Notably, marked inter-individual variation was observed: fish fed the SPCD exhibited significantly lower final body weights and a higher FCR compared with the FMD group (p < 0.001), and pronounced growth divergence was observed between the PB and PS subgroups, with a subset of SPCD-fed fish maintaining growth comparable to fishmeal-fed controls, whereas others exhibited severely constrained growth. Divergent phenotypes were associated with distinct hepatic alterations, including aggravated vacuolation, the enrichment of tight junction-related and immune regulatory pathways, and the broad reprogramming of lipid metabolism. Integrated multi-omics analysis identified arachidonic acid metabolism as the most significantly perturbed pathway, characterized by altered membrane phospholipid composition, the upregulation of RARRES3L, increased COX/LOX-derived eicosanoids, and the suppression of the CYP–EET branch. Collectively, these findings indicate that soy protein replacement induces coordinated hepatic structural and metabolic remodeling, with tight junction disruption and arachidonic acid metabolic reprogramming contributing to inflammatory imbalance and divergent growth phenotypes in T. ovatus.