The multilayered toxic effects of cadmium on earthworms are driven by both cadmium content and soil properties: The potential mediating role of microbiota

Direct Cd exposure remains the dominant driver of mortality and enzyme exhaustion. • Soil microbiota loses diversity, whereas gut microbiota shows structural resilience. • SEM links soil and Cd to host toxicity via microbiomes as potential mediators. • We advocate a multi-tier risk assessment using micro-ecological indicators. Cadmium (Cd) contamination poses substantial risks to soil fauna, yet the combined roles of soil properties and microbial communities in mediating Cd toxicity remain poorly understood. Here, molecular, physiological, and microbiological endpoints were integrated to evaluate multilayered Cd effects on Eisenia fetida across three contrasting soils. Bioavailability assessments showed that soil properties strongly regulated Cd mobility and earthworm accumulation, outperforming total Cd as predictors of toxicity. Cd exposure induced oxidative stress, gene dysregulation, and growth inhibition, with marked soil-dependent variation. Bulk soil microbiota (BSM) and Earthworm gut microbiota (EGM) exhibited distinct but coordinated responses: BSM experienced community disruption, diversity loss, and an increased relative abundance of taxa associated with mobile genetic elements, whereas EGM exhibited structural resilience and an enrichment of putative stress-tolerance traits. Variance decomposition revealed that Cd exposure and soil properties accounted for an average of 53.8% and 46.2% of the explained variance in toxicity-related endpoints, respectively. Structural equation modeling suggested potential indirect pathways linking soil properties and Cd exposure to earthworm growth mediated by microbial communities (standardized effects: −0.68 and −0.17). Overall, Cd toxicity arises from coupled interactions among contamination levels, soil physicochemical traits, and microbial resilience, emphasizing the need to incorporate microbial processes into soil ecotoxicological risk assessments. Download: Download high-res image (294KB) Download: Download full-size image