Unraveling the impact of PFOA toxicity on Zostera marina using a multi-omics approach: Insights from growth, physiological, transcriptomic, and metabolomic signatures

Perfluorooctanoic acid (PFOA), an anthropogenic organic pollutant known for its persistence, resistance to degradation, and toxicity, has raised significant concerns about its potential ecological impacts. Zostera marina, a common submerged seagrass species in temperate offshore areas, is highly vulnerable to pollutant stressors. However, the impact of PFOA on Z. marina remains unclear. In this study, Z. marina was exposed to different concentrations of PFOA (0, 0.5, 1, 5, 10, and 20 μg/L) for 14 days. We subsequently assessed survival rates, growth patterns, physiological indices, transcriptomic profiles, and metabolomic characteristics. The results revealed dose-dependent PFOA accumulation in Z. marina tissues and significant growth inhibition. Furthermore, exposure to PFOA resulted in a significant reduction in photosynthetic pigment content (IBRv2 indices: 2.78-10.29) and elevated enzyme activity (IBRv2 indices: 2.90-8.96). Transcriptomic analysis identified 1511 differentially expressed genes associated with 11 KEGG pathways predominantly affected by PFOA exposure. Weighted gene co-expression network analysis highlighted the crucial role of the hydroxyphenylpyruvate reductase (hppr) gene in antioxidant defense mechanisms and detoxification processes against PFOA-induced stress. Metabolomics identified 412 differentially expressed metabolites, mainly consisting of flavonoids, organic acids, and lipids. In summary, PFOA exposure resulted in the down-regulation of gene expression related to photosynthesis and energy metabolism while also affecting metabolite synthesis. The response of Z. marina to PFOA stress involves modulation of the cytoskeletal dynamics and signal transduction pathways, as well as activation of a suite of genes and metabolites to initiate defense mechanisms.