Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome

Abstract

Significance The root microbiome composition is largely determined by the soil inoculum, with a distinct contribution from the host. The molecular mechanisms with which the host influences its rhizobiome are only beginning to be discovered. Using a hydroponics-based synthetic community approach, we probe how root-exuded specialized metabolites sculpt the root microbiome. We uncover a role for coumarins in structuring the rhizobiome, particularly by limiting the growth of a Pseudomonas strain, for which we propose a mechanism of action involving reactive oxygen species. Our findings support the possibility that root-exuded coumarins form a part of the plant’s adaptive response to iron deficiency that goes beyond iron mobilization to modulate the rhizobiome, and highlight avenues toward engineering the rhizosphere for plant health. The factors that contribute to the composition of the root microbiome and, in turn, affect plant fitness are not well understood. Recent work has highlighted a major contribution of the soil inoculum in determining the composition of the root microbiome. However, plants are known to conditionally exude a diverse array of unique secondary metabolites, that vary among species and environmental conditions and can interact with the surrounding biota. Here, we explore the role of specialized metabolites in dictating which bacteria reside in the rhizosphere. We employed a reduced synthetic community (SynCom) of Arabidopsis thaliana root-isolated bacteria to detect community shifts that occur in the absence of the secreted small-molecule phytoalexins, flavonoids, and coumarins. We find that lack of coumarin biosynthesis in f6′h1 mutant plant lines causes a shift in the root microbial community specifically under iron deficiency. We demonstrate a potential role for iron-mobilizing coumarins in sculpting the A. thaliana root bacterial community by inhibiting the proliferation of a relatively abundant Pseudomonas species via a redox-mediated mechanism. This work establishes a systematic approach enabling elucidation of specific mechanisms by which plant-derived molecules mediate microbial community composition. Our findings expand on the function of conditionally exuded specialized metabolites and suggest avenues to effectively engineer the rhizosphere with the aim of improving crop growth in iron-limited alkaline soils, which make up a third of the world’s arable soils.