Asymmetric Microbial Succession Drives Soil Multifunctionality Recovery over a 25 Year Chronosequence of Rare Earth Tailings Restoration

Soil microorganisms sustain critical soil functions, yet the specific contributions of bacterial and fungal communities to multifunctionality during natural succession in rare earth element (REE) mining tailings remain poorly understood. We characterized bacterial and fungal succession dynamics and their impacts on soil multifunctionality, encompassing C, N, P, and K cycling, along a 10-, 18-, and 25 year natural restoration chronosequence in REE tailings. Our results demonstrate that individual soil functions and overall multifunctionality increased significantly by 76-596% and 14.4-fold, respectively, with restoration time. Restoration-driven shifts in bacterial community composition (correlation coefficients: <i>r</i> = -0.776-0.919) and fungal co-occurrence patterns (<i>r</i> = -0.818-0.814) strongly correlated with enhanced multifunctionality. Fungal communities exhibited greater resilience than bacterial communities during succession, with heterotrophic taxa including Actinobacteriota (e.g., <i>Frankia</i>) and Basidiomycota (e.g., <i>Amphinema</i> and <i>Scleroderma</i>) becoming enriched in 25 year restored sites, contrasting sharply with oligotrophic microbes (Myxococcota, Chloroflexi, and <i>WPS-2</i>) that declined. Furthermore, fungal networks showed reduced modularity as restoration progressed, reflecting weaker niche differentiation. Structural equation modeling revealed a slightly stronger fungal regulation of multifunctionality (total effect: 0.108) compared to bacteria (0.086). This was mediated through the enrichment of Actinobacteriota, depletion of oligotrophic groups (<i>WPS-2</i> and Myxococcota), and synergistical fungal interactions involving taxa like <i>Cladophialophora</i>, <i>Amphinema</i>, and <i>Scleroderma</i>. This study highlights the potential of engineering synthetic microbial consortia based on these keystone taxa to accelerate restoration of metal-contaminated ecosystems.