Co-functioning of bacterial exometabolites drives root microbiota establishment

Soil-dwelling microbes are the principal inoculum for the plant microbiota, but the role of microbe-microbe interactions in microbiota establishment remains fragmentary. We tested 39,204 binary interbacterial interactions for inhibitory activities in vitro, allowing us to identify taxonomic signatures in the inhibitory profiles of individual bacteria. Using genetic and metabolomic approaches, we identified the antimicrobial 2,4-diacetylphloroglucinol and the iron-chelator pyoverdine as exometabolites whose combined functions explain most of the inhibitory activity of the strongly antagonistic Pseudomonas brassicacearum R401. Microbiota reconstitution with a core of Arabidopsis thaliana root commensals in the presence of wild-type or mutant strains revealed a root niche-specific co-function of these exometabolites as root competence determinants and drivers of predictable changes in the root-associated community. In natural environments, both corresponding biosynthetic operons are enriched in roots, a pattern likely linked to their role as iron sinks, indicating that these co-functioning exometabolites contribute to Pseudomonad pervasiveness throughout the root microbiota.