Environmental PCB1254 exposure impairs shrimp survival, gut health, and nutritional quality via oxidative stress and ferroptosis

Polychlorinated biphenyls (PCBs) are persistent organic pollutants commonly found in coastal aquaculture waters, posing significant threats to aquatic ecosystems and food safety. Understanding their toxic effects on edible species like Litopenaeus vannamei shrimp is crucial for sustainable aquaculture and protecting human consumers. Current knowledge often lacks a comprehensive, multi-level understanding of PCB toxicity, particularly concerning their impact on oxidative stress, metabolic pathways, and gut microbiota, which are critical for organismal health and resilience.

Researchers conducted a 14-day subchronic waterborne exposure of Litopenaeus vannamei shrimp to environmentally relevant concentrations of 1 ng/L and 10 ng/L PCB1254. The study utilized integrated multi-omics techniques, including histology, lipid peroxidation assays, redox homeostasis markers, gene expression analysis (qPCR), metabolomics, and intestinal microbiota sequencing, to systematically explore toxicological effects across different biological levels. Control groups were maintained without PCB exposure.

Exposure to PCB1254 significantly reduced shrimp survival and impaired ammonia stress tolerance. Histological alterations and oxidative stress were observed in the gills, evidenced by the accumulation of lipid peroxidation products and disruption of redox homeostasis. Ferroptosis homeostasis in the gills was also affected, with induced iron accumulation and altered expression of gene markers. The study found disturbed expression of antimicrobial peptide genes (e.g., ALF, Pen3) and increased expression of inflammation-related genes (e.g., JNK, TNFα). Metabolic patterns in the gills were disrupted, particularly in amino acid metabolism and ABC transporters pathways, alongside changes in arachidonic acid and tryptophan metabolites. Intestinal histological morphology was damaged, and microbial communities were disturbed, showing reduced diversity and altered abundance of functional bacteria (e.g., Vibrio, Pseudoalteromonas, Bacteroides, Lactobacillus).

Intestinal metabolic functions were also disrupted, including carbohydrate absorption and β-lactam resistance. Finally, the nutritional value of muscle was impaired, with reductions in crude protein, total amino acids, and delicious amino acids.