Toxic effects of environmental-level polychlorinated biphenyls on Litopenaeus vannamei: Multi-omics integration of oxidative stress, ferroptosis, metabolism, intestinal microbiota, and nutritional quality

Polychlorinated biphenyls (PCB) are typical persistent organic pollutants widely present in the environment, which commonly contaminate coastal aquaculture waters. Clarifying their toxic effects on edible shrimp is of great significance for healthy aquaculture development and food safety. This study conducted a 14-day subchronic exposure of Litopenaeus vannamei to 1 ng/L and 10 ng/L PCB1254 via waterborne exposure simulating environmental pollution levels, and systematically explored the toxicological effects of PCB at different biological levels using integrated multi-omics techniques. The results showed that PCB exposure reduced the survival and ammonia stress tolerance of the shrimp, and induced histological alterations and oxidative stress in the gills, manifested as the accumulation of lipid peroxidation products and the disruption of redox homeostasis. It affected ferroptosis homeostasis in the gills by inducing iron accumulation and altering the expression of gene markers, disturbed the expression of antimicrobial peptide genes (e.g., ALF , Pen3 ), and increased the expression of inflammation-related genes (e.g., JNK , TNFα ). Furthermore, the metabolic patterns in the gills were also disrupted, especially the pathways of amino acid metabolism and ABC transporters, as well as arachidonic acid and tryptophan metabolites. In addition, intestinal histological morphology was damaged, and microbial communities were disturbed, manifested as reduced diversity, altered abundance of functional bacteria (e.g., Vibrio , Pseudoalteromonas , Bacteroides and Lactobacillus ), and disrupted metabolic functions (e.g., carbohydrate absorption, β -lactam resistance). Finally, the nutritional value of the muscle was impaired by reducing the contents of crude protein, total amino acids and delicious amino acids. In conclusion, this study revealed that exposure to environmentally relevant concentrations of PCB-1254 induced toxic effects on shrimp by triggering histological alterations, oxidative stress, ferroptosis, metabolic reprogramming and intestinal microbiota disorder, and altered their muscle nutritional quality.