Perfluorobutane sulfonate (PFBS) disrupts earthworm reproduction via DNA damage, metabolic collapse, and oxidative stress

Perfluorobutane sulfonate (PFBS) is a persistent environmental contaminant, frequently found leaking into soils from landfill leachates and wastewater due to inefficient removal processes. Despite its widespread presence, the precise mechanisms underlying its reproductive toxicity in soil fauna, particularly invertebrates like earthworms, remain poorly understood. This knowledge gap is critical, as earthworms play a vital role in soil health and ecosystem function, making them key indicators of environmental pollution. Understanding PFBS's impact on their reproduction is essential for assessing ecological risk and developing effective remediation strategies.

Researchers exposed Eisenia fetida earthworms to PFBS at concentrations of 0.1, 1, and 10 mg/kg in soil for a 28-day period. The study assessed reproductive endpoints including cocoon number, size, and aspect ratios, as well as sperm counts in the seminal vesicle and chromatin status of spermathecae. Histopathological examination focused on structural damage to sperm cysts in the clitellum. To elucidate mechanisms, transcriptomics and metabolomics analyses were performed on clitellum tissue, alongside measurements of oxidative stress biomarkers such as CAT, POD, GST activities, and MDA levels.

PFBS exposure significantly impaired reproductive parameters in Eisenia fetida. The study observed reduced cocoon number, size, and aspect ratios, alongside a notable decrease in sperm counts within the seminal vesicle. Furthermore, chromatin depletion was evident in spermathecae, and structural damage to sperm cysts in the clitellum was confirmed. Transcriptomic analysis revealed widespread dysregulation of key pathways: WNT, protein digestion/absorption, and NF-κB pathways were altered across all PFBS concentrations. At the highest dose of 10 mg/kg PFBS, oxytocin and oocyte meiosis pathways were also significantly affected. Metabolomics data indicated a concerted collapse of several metabolic networks in the clitellum, including energy metabolism, amino acid metabolism, nucleotide metabolism, and carbohydrate metabolism.

Expression levels of ATP6, TRIAP1, CYP450, TCTP, and CCF-1 were up-regulated, suggesting a compensatory response to environmental stress, though the biphasic responses of ANN indicated limited regulatory capacity. Additionally, PFBS triggered significant oxidative stress in the clitellum, with CAT activity, POD activity, GST activity, and MDA levels all significantly altered (P < 0.05). These findings collectively point to DNA repair failure, metabolic network sabotage, and redox imbalance as key mechanisms of PFBS-induced reproductive toxicity.