Chain length-dependent toxicity of PFAS in tomato: Linking rhizosphere microbiota to host oxidative damage through metabolic reprogramming

Per- and polyfluoroalkyl substances (PFAS) are a class of persistent environmental pollutants that pose significant threats to plant health and ecosystem stability. However, the molecular mechanisms underlying their toxicity, particularly how carbon chain length influences biological effects, remain poorly understood. This study employed an integrated multi-omics approach to systematically investigate the toxicity mechanisms of PFAS in the soil-plant system. We find that PFAS exposure inhibits tomato seedling growth, inducing reactive oxygen species accumulation and membrane lipid peroxidation damage. Molecular docking revealed that perfluorooctanoic acid (PFOA) exhibited stronger binding affinity to superoxide dismutase (SOD, −7.6 kcal/mol) and glutathione (GSH, −7.8 kcal/mol) compared to perfluorobutanoic acid (PFBA, −5.2 and −6.0 kcal/mol). Rhizosphere microbial analysis demonstrated PFAS-driven community restructuring, with PFOA treatments increasing Pseudomonadota abundance by 157% and Bacillota by 185%. Metabolomics identified 704 differentially expressed metabolites, showing PFAS suppressed fatty acid metabolism while activating ABC transporters and antioxidant biosynthesis. Random forest identified 15 key biomarkers for oxidative damage, including microbial genera ( Methylibium , Thauera ) and plant metabolites (Tomatine). This research elucidates the chain length-dependent toxicity mechanisms of PFAS across molecular, microbial, and metabolic dimensions, providing critical biomarkers for ecological risk assessment and remediation strategies.