Key metabolite-mediated rhizosphere microenvironment reconstruction alleviates resource limitation during bauxite residue pedogenesis

Transforming highly alkaline, nutrient-poor bauxite residue (BR) into functional soil (pedogenesis) requires establishing intricate feedback loops between pioneer plants and the microbiome. However, the molecular mechanisms driving microbial resource and metabolic coupling during this engineered pedogenesis remain poorly understood. To decode these mechanisms, we conducted an pot experiment using Elymus dahuricus and combined amendments (ferrous sulfate, citric acid, nitrohumic acid), integrating physicochemical profiling with multi-omics (microbiome sequencing, FT-ICR MS, and LC-MS) to evaluate rhizosphere eco-physiological responses. Combined treatments significantly mitigated extreme BR alkalinity (pH decreased from 10.1 to 8.5) and activated nutrient cycling (e.g, microbial biomass C, N, and P increased from 1.9, 0.4, 5.5 mg kg –1 to 7.1, 9.9, 95.9 mg kg –1 , respectively). Crucially, this environmental amelioration shifted microbial life strategies from stress-tolerant to growth-oriented communities, significantly enhancing microbial carbon use efficiency (CUE). Multi-omics analyses revealed that plant colonization enriched labile, low-molecular-weight dissolved organic matter, whereas amendments introduced stable, degradation-resistant organics. Random Forest and structural equation modeling (PLS-PM) further elucidated that plant-driven shifts in microbial strategies regulated the accumulation of key plant-associated metabolites (e.g., Capsiate and Isomasticadienonalic acid). Ultimately, these key metabolites reconstructed the rhizosphere microenvironment by enriching labile carbon, which directly alleviated the enzymatic stoichiometric resource limitations of the microbiome. These findings provide novel molecular evidence that manipulating rhizosphere metabolic chemodiversity is essential for overcoming extreme alkalinity and N/P deficiency. Regulating these plant-microbe-metabolite feedbacks represents a critical biological pathway for accelerating the ecological reconstruction of extreme industrial residues. • Microbial strategies shifted from stress-tolerance to high-growth yield • Increased microbial CUE derives from the alleviated N/P limitations • Pasture establishment and humus addition enhanced molecular-level biodiversity of DOM • Capsiate and terpenoids identified as key signaling metabolites triggering plant growth • Key metabolite-mediated microenvironment reconstruction alleviates N/P limitation