The chemical ecology of coumarins and phenazines affects iron acquisition by pseudomonads

Secondary metabolites are important facilitators of plant-microbe interactions in the rhizosphere, contributing to communication, competition, and nutrient acquisition. However, at first glance, the rhizosphere seems full of metabolites with overlapping functions, and we have a limited understanding of basic principles governing metab- olite use. Increasing access to the essential nutrient iron is one important, but seem- ingly redundant role performed by both plant and microbial Redox-Active Metabolites (RAMs). We used coumarins, RAMs made by the model plant Arabidopsis thaliana, and phenazines, RAMs made by soil-dwelling pseudomonads, to ask whether plant and microbial RAMs might each have distinct functions under different environ- mental conditions. We show that variations in oxygen and pH lead to predictable differences in the capacity of coumarins vs phenazines to increase the growth of iron-limited pseudomonads and that these effects depend on whether pseudomonads are grown on glucose, succinate, or pyruvate: carbon sources commonly found in root exudates. Our results are explained by the chemical reactivities of these metab- olites and the redox state of phenazines as altered by microbial metabolism. This work shows that variations in the chemical microenvironment can profoundly affect secondary metabolite function and suggests plants may tune the utility of microbial secondary metabolites by altering the carbon released in root exudates. Together, these findings suggest that RAM diversity may be less overwhelming when viewed through a chemical ecological lens: Distinct molecules can be expected to be more or less important to certain ecosystem functions, such as iron acquisition, depending on the local chemical microenvironments in which they reside.

Automated summary

Secondary metabolites play important roles in plant-microbe interactions in the rhizosphere, contributing to communication, competition, and nutrient acquisition. The study investigates the distinct functions of plant and microbial Redox-Active Metabolites (RAMs) in different environmental conditions, focusing on the capacity of coumarins and phenazines to increase the growth of iron-limited pseudomonads. The results highlight the profound impact of chemical microenvironments on secondary metabolite function and suggest the ability of plants to tune the utility of microbial secondary metabolites by altering carbon released in root exudates.