Ecotype-Specific Drilosphere Microbiome Reprogramming Influencing Microplastic Impacts on Soil Carbon–Nitrogen Characteristics and Earthworm Health

The soil drilosphere is a critical biogeochemical hotspot, yet its role as a key interface for microplastic (MP) accumulation and impact remains poorly characterized. We investigated how polyethylene microplastics (<150 μm) affect the drilosphere compartments (gut, burrows, and casts) of two distinct earthworm ecotypes: epigeic Eisenia fetida and endogeic Pheretima guillelmi . Results showed that MPs significantly enrich in the drilosphere compared to bulk soil, with the endogeic species exhibiting greater accumulation. While earthworm activity typically stimulated nutrient characteristics, MP exposure disrupted these functions, significantly reducing total nitrogen (5.0–25.0%) and ammonium (28.5–62.1%). Ecotype-specific host damage emerged: E. fetida exhibited pronounced immune and oxidative stress responses, whereas P. guillelmi suffered severe digestive and metabolic impairments. These impacts were mediated by distinct microbiome reprogramming. MP-induced dysbiosis intensified progressively along the soil–drilosphere–gut continuum. Multivariate and transcriptomic analyses revealed that external-drilosphere microbiota shifts drove carbon–nitrogen characteristic alterations, while internal dysbiosis triggered host physiological stress. This study highlights that ecotype-specific restructuring of drilosphere microbiomes underpins the ecosystem-scale impacts of MP pollution, demonstrating that earthworm functional diversity is essential for comprehensive soil health risk assessments.