Centennial Pb-Zn mining pollution: Spatial distance impacts on agricultural soil microbiota stress response

Mining activities pose significant threats to agricultural ecosystems through heavy metals (HMs) contamination, particularly in acidic red soils. Since there was limited research on the response mechanisms of agricultural microorganisms at different distances within typical mining areas to HMs stress, This study investigated HMs pollution patterns, microbial community dynamics, and functional gene responses in farmland surrounding a century-old Pb-Zn mine in Shuikoushan, Hengyang City, China. Soil samples were collected from three zones: Short-Distance (SD, 0-10 km), Medium-Distance (MD, 10-15 km), and Long-Distance (LD, 15-25 km) from the mine. Results revealed a pronounced distance-dependent decline in composite HMs pollution, with Cd (R²=0.61) and As (R²=0.51) showing the strongest correlations to proximity. SD zone exhibited severe contamination, with Cd (8.25 ± 5.74 mg kg⁻¹) and As (58.58 ± 49.63 mg kg⁻¹) concentrations exceeding regulatory limits by 27.5 and 1.95 fold, respectively. Bacterial diversity demonstrated significant spatial stratification, with Shannon indices increasing from SD to LD zones (6.8→7.2), while β-diversity decreased, indicating reduced ecological heterogeneity at lower pollution levels. High HMs stress in SD zone favored anaerobic taxa like Thermomarinilinea and acid-tolerant phyla like Acidobacteriota, whereas aerobic taxa like Gaiella dominated less-polluted areas. Metagenomic analysis revealed upregulation of HMs resistance genes (czcABCD, cadCD, arsABCJR) in SD zone. Correlation network analysis highlighted intensified positive interactions among bacterial genus under HMs stress, suggesting cooperative survival strategies. These findings elucidate the dual pressure of HMs toxicity and soil acidification on microbial ecosystems, providing critical insights for ecological risk assessment and bioremediation strategies in mining-impacted agricultural lands. The study underscores the need for distance-based pollution control measures and highlights microbial genetic adaptation as a potential tool for rehabilitating heavy metal-contaminated red soils.