Foliar metal micronutrients reshape rhizosphere soil multifunctionality by filtering microbial life-history strategies.

Abstract

Foliar application of metal micronutrients is increasingly adopted in intensive cultivation systems, yet its potential ecological risks to rhizosphere functions remain poorly understood. Here, using the medicinal plant Panax notoginseng as a model, we conducted a gradient foliar amendment experiment with iron (Fe), zinc (Zn), and copper (Cu) to evaluate how aboveground metal inputs regulate rhizosphere soil multifunctionality (MF) through microbial life-history strategies. By integrating 16S rRNA amplicon sequencing, metagenomics, root transcriptomics, and a newly developed quantitative Yield-Acquisition-Stress tolerance (qYAS) framework, we disentangled the microbial mechanisms underlying divergent functional responses to metal amendments. Foliar Fe significantly enhanced multifunctionality, including nutrient provision and element cycling, while Cu and Zn reduced nutrient provision and element cycling, but enhanced plant pathogen abundances. These changes were closely associated with shifts in bacterial life-history strategies: Fe promoted Y-strategists characterized by efficient carbon use, streamlined genomes, and high network connectivity, whereas Cu and Zn enriched AS-strategists with larger genomes and negative associations with multifunctionality. Partial least squares path modeling (PLS-PM) further identified microbial strategies as key mediators linking foliar metal inputs, plant performance, soil properties, and multifunctionality. This study provides a trait-based microbial framework for evaluating foliar metal fertilization and guiding safer nutrient management.