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: r = −0.776–0.919) and
fungal co-occurrence patterns (r = −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., Frankia) and Basidiomycota (e.g., Amphinema and Scleroderma) becoming enriched in 25 year restored sites, contrasting sharply
with oligotrophic microbes (Myxococcota, Chloroflexi, and WPS-2) 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 (WPS-2 and Myxococcota), and synergistical fungal interactions involving
taxa like Cladophialophora, Amphinema, and Scleroderma. This study highlights the potential of engineering synthetic microbial
consortia based on these keystone taxa to accelerate restoration of
metal-contaminated ecosystems.