Heterogeneous distribution of toxic arsenic modulates the mutualistic interaction between Pteris vittata and soil microbiota

While soil nutrient heterogeneity is known to influence plant fitness and ecosystem diversity, the ecological effects of heterogeneous arsenic (As) contamination on plant-microbe interactions remain unclear. Using multi-omics, we demonstrate that the As-hyperaccumulator Pteris vittata restores diminished microbial alpha diversity under As heterogeneity. The plant actively forages As by proliferating roots in As-rich patches and altering its root exudate profile. Key exudates, such as phosphocholine and N-acetyl histamine, recruit specific microbial taxa, such as class KD4-96, and order Vicinamibacteraceae, which upregulate As-transforming genes and enhance As mobilization. Rhizobacteria including Blastococcus and Streptomyces also produce auxin, stimulating root growth. Together, these responses form a self-reinforcing feedback loop-linking root foraging, microbial recruitment, As mobilization, and root elongation-that amplifies plant growth and arsenic uptake. Our work establishes a rhizosphere engineering strategy to leverage such plant-microbe feedbacks for improved phytoremediation.