Tire wear particles (TWPs), generated from tire abrasion, contribute significantly to environmental contamination. The toxicity of TWPs to organisms has raised significant concerns, yet their effects on terrestrial plants remain unclear. Here, we investigated the long-term impact of pristine and naturally aged TWPs on water spinach (Ipomoea aquatica) and its rhizospheric soil. The results indicated that natural aging reduced the toxicity of TWPs, as evidenced by decreased levels of polycyclic aromatic hydrocarbons (PAHs) in soil and TWPs themselves. Consequently, aged TWPs were found to enhance the plant growth and chlorophyll content, whereas pristine TWPs increased the plant stress. Furthermore, aged TWPs improved soil organic matter (SOM) and total organic carbon (TOC), thereby boosting the microbial enzymes involved in nitrogen cycling. Metabolomic analysis revealed that aged TWPs upregulated key pathways related to carbon and nitrogen metabolism, enhancing plant growth and stress responses. Additionally, rhizosphere bacterial diversity was higher under aged TWPs, favoring nutrient-cycling taxa such as Acidobacteriota and Nitrospirota. Pristine TWPs may lead to overproliferation of certain dominant species, thereby reducing microbial diversity in soil, which could ultimately compromise the soil health. These findings contribute to a deeper understanding of the mechanisms underlying TWP toxicity in plants and highlight the necessity for further research on the impact of aged TWPs across various plant species over different exposure durations for comprehensive risk assessment.
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