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Functional decoupling between plant remediation efficacy and microbial metal resistance in iron tailings: A Robinia pseudoacacia-driven paradox.

Jiaying Liu,Weixi Zhang,Ran Wang,Siqi Wu,Xuejiao Bai,Xuejing Wang,Wenxu Zhu,Changjun Ding

Published 2026 in Ecotoxicology and Environmental Safety

ABSTRACT

Mining-derived iron tailings pose severe ecotoxicological risks through soil degradation and persistent heavy metal contamination. This study evaluates the ecorestoration potential of three tree species-Populus davidiana, Robinia pseudoacacia, and Rhus typhina-in iron tailings from China's Huluyu Iron Mine. Using an integrated assessment combining soil quality index (SQI), enzymatic activities, metagenomics, and partial least squares path modeling (PLS-PM), we demonstrate that Robinia pseudoacacia achieved the highest SQI (0.68) by significantly mitigating metal stress, which was associated with a marked reduction in soil pH (to 6.29). This acidification is consistent with the well-documented role of root exudates in legumes, alongside enhancing nutrient accumulation (total carbon: 24.8 g/kg; total nitrogen: 1.5 g/kg), and stimulating sucrase and phosphatase activities. Paradoxically, Robinia pseudoacacia soils exhibited minimal enrichment of microbial metal resistance genes, challenging the prevailing "Rhizosphere Synergy Hypothesis." Instead, Robinia pseudoacacia's efficacy relied on functional decoupling from microbial metal detoxification pathways, favoring metabolic optimization of carbon/nitrogen cycling and organic acid-driven pH regulation. PLS-PM confirmed soil chemical properties (pH, total carbon, nitrogen) and enzymatic activities as direct positive drivers of SQI (p < 0.05), while heavy metal content exerted significant negative effects (r = -0.55, p < 0.001). These findings establish RP as an optimal species for iron tailings restoration, reconciling soil fertility enhancement with a potential reduction in metal bioavailability mediated by soil acidification. We propose a predictive SQI framework for selecting remediation species in metalliferous environments, offering critical insights into sustainable management of mining-associated ecotoxicological risks.

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