Rhizobacteria opportunistically boost colonization and impair plant fitness by degrading plant-derived coumarins under iron deficiency

Abstract Plants recruit root-associated bacterial assemblies primarily through the secretion of specialized metabolites, and the resultant rhizospheric microbiota is empirically considered beneficial. However, detrimental effects on plants arising from bacterial colonization that exploits plant-derived metabolites are rarely documented. Here, we demonstrate that the rhizosphere-derived Pseudomonas sp. strain NyZ480 exhibits a versatile capacity to effectively degrade and utilize simple coumarins — a class of root exudates essential for plant iron acquisition and pathogen defense. This robust catabolic capability is mediated by conserved genetic determinants in NyZ480. In particular, redundant degradation-initiating xenA genes confer NyZ480 not only growth using simple coumarins but also resistance to these antimicrobial metabolites. Consequently, NyZ480 significantly colonizes iron-stressed, coumarin-secreting Arabidopsis roots, trapping plants in perpetual iron scarcity and progressively compromising iron acquisition and overall fitness. Bioinformatic analyses indicate that xenA homologs are prevalent and redundant in environmental bacteria. Thus, we reveal a rhizospheric phenomenon where microorganisms opportunistically utilize and detoxify host-secreted specialized metabolites under stress conditions, enhancing colonization and impairing plant fitness.