Tire Wear Particles Drive a Systemic Bioenergetic Collapse in Eisenia fetida via Coupled Barrier Erosion and Metabolic-Immune Dysregulation

Abstract While electric vehicles can mitigate exhaust emissions, their greater mass and rapid torque accelerate tire wear particle (TWP) emissions, threatening soil ecosystems. However, whether TWPs systemically undermine the physiological integrity of soil organisms remains unclear. Here, we demonstrate that TWPs induce systemic bioenergetic collapse in the earthworm Eisenia fetida. TWPs disrupted biological barriers through synergistic physical abrasion and chemical leaching. This structural collapse manifested histologically as epidermal sloughing and intestinal villous atrophy, accompanied by an increase in mucus coverage from 1.77 to 3.96%, and molecularly as synchronized transcriptional suppression of extracellular matrix networks. Continuous toxic leachate influx overwhelmed detoxification pathways, triggering severe oxidative stress. Faced with this persistent dual threat, earthworms adopted an unsustainable physiological trade-off. They drastically suppressed key nutrient assimilation, as evidenced by a 33.9–47.8% reduction in lipase activity, and reallocated limited energy resources to lipid-driven inflammatory defenses. This critical energy shift ultimately disrupted the PI3K-Akt survival signaling pathway and precipitated immunosuppressive exhaustion. Consequently, this lethal metabolic-immune dysregulation triggered a rapid wasting syndrome characterized by weight loss exceeding 0.3 g and up to 40% mortality. Our findings redefine TWP toxicity as an energy allocation crisis, highlighting an underestimated ecological vulnerability associated with modern traffic emissions.