Cooperative siderophore use stabilizes a protective leaf microbiome

Plant-associated microbial communities provide crucial protection against pathogens. Specialized metabolites play key roles in plant-microbe and microbe-microbe interactions and, ultimately, in plant health; however, the molecular mechanisms underlying their plant-protecting properties remain largely unknown. Nutrient deficiency (e.g., iron) on leaf surfaces creates intense competition among microbes, driving both antagonism and cooperation. Using a gnotobiotic <i>Arabidopsis thaliana</i> model and a synthetic leaf microbial community, we show that community stability and plant protection depend on cooperative siderophore exchange between the basidiomycete yeast <i>Rhodotorula kratochvilovae</i> and commensal <i>Pseudomonas</i> species. Removal of <i>Pseudomonas</i> caused a strong shift in the community metabolome and accumulation of the yeast siderophore rhodotorulic acid (RA). RA selectively promoted the growth of commensal <i>Pseudomonas</i> via TonB-dependent transporters, which are absent in pathogenic <i>Pseudomonas</i> strains. Inactivation of these transporter genes abolished RA uptake, destabilized the synthetic community, and eliminated protection against <i>Pseudomonas syringae</i> infection. RA and <i>Rhodotorula</i> also induced host iron-deficiency and jasmonate-related defense metabolites, linking microbial cooperation to plant stress responses. These findings reveal that microbial siderophore exchange acts as a key mechanism that maintains stability in the phyllosphere microbiome. Rather than solely promoting competition, iron-binding compounds can serve as cooperative currencies that align microbial fitness with host protection.