Unveiling the interactions of 8:2 fluorotelomer sulfonic acid (8:2 FTSA) with the earthworm-microbe symbiosis in soil.

8:2 fluorotelomer sulfonic acid (8:2 FTSA), an important per- and polyfluoroalkyl substance (PFAS) found in aqueous film-forming foams (AFFFs), is frequently detected in soil. However, the interactions of 8:2 FTSA with soil-terrestrial invertebrate systems are poorly understood. This study investigated the biotransformation, toxicity, microbiome shifts, and microbial degradation of 8:2 FTSA in a soil-earthworm system through in vivo, in vitro, and multi-omics analyses. Earthworms efficiently accumulated 8:2 FTSA and biotransformed it into 11 distinct PFAS via α/β-oxidation mediated by metabolic enzymes, with trifluoroacetic acid (TFA) as the predominant metabolite. 8:2 FTSA induced significant oxidative stress, activated metabolic detoxification, and caused potential neurotoxic effects in earthworms. Furthermore, 8:2 FTSA exposure disrupted the microbial communities in the earthworm-soil system, with greater sensitivity observed in communities on the earthworm skin and in the soil compared to those in the gut. Predicted functional profiling further suggested that the gut microbiota may have greater potential for xenobiotic transformation, whereas the skin microbiota exhibited a host-dependent and low-activity phenotype. Raoultella ornithinolytica, isolated from earthworm gut and skin, transformed over 68% of 8:2 FTSA in 6 days via α/β-oxidation. Our findings advance the understanding of 8:2 FTSA interactions with the soil-earthworm system and provide a critical foundation for assessing its ecological risk in terrestrial environments.