A cell-free bacterial signal orchestrates trans-kingdom fitness tradeoff to enhance sulfur deficiency tolerance in plants

Plant-associated microorganisms interact with each other and host plants via intricate chemical signals, offering multiple benefits, including plant nutrition. We report such a mechanism through which the rhizosphere microbiome improves plant growth under sulfur (S) deficiency. Disruption of plant S homeostasis resulted in a coordinated shift in composition and S-metabolism of the rhizosphere microbiome. Using this insight, we developed an 18-membered synthetic rhizosphere bacterial community (SynCom) that rescued growth of Arabidopsis and a leafy Brassicaceae vegetable under S-deficiency. This beneficial trait is taxonomically widespread among SynCom members, with bacterial pairs predominantly providing synergistic benefits to host plants. Notably, stronger competitive interactions among SynCom members conferred greater fitness benefits to the host, suggesting a trans-kingdom fitness tradeoff. Finally, guided chemical screening, deletion knockout mutant, and targeted metabolomics identified and validated microbially released glutathione (GSH) as the necessary bioactive signal that orchestrates plant-microbe (trans-kingdom) fitness tradeoff and improves plant growth under sulfur limitation. HighlightsO_LIAlteration in plant sulfur (S) homeostasis leads to coordinated shifts in the composition and S-metabolism of the rhizosphere microbiome. C_LIO_LITaxonomically divergent bacterial members within the rhizosphere microbiome improve plant growth under S-deficiency. C_LIO_LIStronger competitive interactions within rhizosphere bacterial members provide greater fitness benefit to the host plant under S-deficiency, suggesting a trans-kingdom fitness tradeoff. C_LIO_LIMicrobially released glutathione (GSH) is a necessary bioactive signal that improves plant growth under sulfur limitation and orchestrates plant-microbe (trans-kingdom) fitness tradeoff. C_LI