Root Metabolic Shifts Drive Genome-Resolved Cometabolism of Phthalates and Coupled Humification in Mollisols

Extensive import of mixed phthalate esters (PAEs) threatens Mollisol ecosystems. Nevertheless, mechanisms through which plant roots orchestrate the cometabolic degradation of PAEs and couple this with soil humification remain unclear. This study integrated plant physiology, untargeted metabolomics, and genome-resolved metagenomics to decipher response trajectories of the Pak Choi-Mollisol root-microbe system across a mixed PAEs gradient. The findings indicated that under mild stress (5 mg/kg), plants sustained a "growth-driven" homeostasis alongside a stable rhizospheric microbiome. In contrast, acute toxicity (20 mg/kg) initiated pronounced metabolic shifts, characterized by a "survival-overgrowth" strategy. Specifically, carbon fluxes shifted from primary assimilation to secondary defense hubs. This physiological tradeoff reversed the root exudate profile, shifting from basic carbohydrates to massive efflux of specific organic acids and phenolics. Critically, these allelochemicals functioned as exogenous elicitors, selectively recruiting specific metagenome-assembled genomes (MAGs). Genomic evidence confirmed that single keystone MAGs (Pseudomonas and Burkholderia) coharbored pcaG/H and extracellular laccase genes, establishing a self-contained cometabolic module for concurrent PAEs degradation and carbon stabilization. Consequently, based on correlative multiomics evidence, extensive carbon efflux was associated with a putative coupling between PAEs detoxification and stable humic carbon accumulation, as indicated by a 48.7% increase in the humification index (HIX). Ultimately, this multiomics framework elucidates the plant-driven enhancement of carbon sinks within contaminated soils.