The chemical ecology of coumarins and phenazines affects iron acquisition by pseudomonads
Abstract
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 metabolite use. Increasing access to the essential nutrient iron is one important, but seemingly 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 environmental 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 metabolites 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.
Additional Information
© 2023 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). We thank S. Wilbert for help with dissolved oxygen measurements. This work was supported by a grant from the NIH (1R01AI127850-01A1) to D.K.N. D.L.M. was supported by a division postdoctoral fellowship from Biology and Biological Engineering at Caltech, the Simons Foundation Marine Microbial Ecology postdoctoral fellowship and the L'Oréal USA for Women in Science postdoctoral fellowship. Author ContributionsD.L.M. and D.K.N. designed research; D.L.M. and J.L. performed research; D.L.M., J.L. and D.K.N. analyzed data; and D.L.M. and D.K.N. wrote the paper. Data, Materials, and Software Availability. All study data are included in the article and/or SI Appendix. The authors declare no competing interest.Attached Files
Published - pnas.2217951120.pdf
Supplemental Material - pnas.2217951120.sapp.pdf
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Additional details
- PMCID
- PMC10083548
- Eprint ID
- 121674
- Resolver ID
- CaltechAUTHORS:20230602-251523000.6
- 1R01AI127850-01A1
- NIH
- Caltech Division of Biology and Biological Engineering
- Simons Foundation
- L'Oreal USA For Women in Science Fellowship
- Created
-
2023-06-12Created from EPrint's datestamp field
- Updated
-
2023-06-20Created from EPrint's last_modified field
- Caltech groups
- Division of Geological and Planetary Sciences, Division of Biology and Biological Engineering