Experiments using an ecologically realistic 185-member bacterial synthetic community in the root system ofArabidopsisreveal thatVariovoraxbacteria can influence plant hormone levels to reverse the inhibitory effect of the community on root growth. Plants grow within a complex web of species that interact with each other and with the plant(1-10). These interactions are governed by a wide repertoire of chemical signals, and the resulting chemical landscape of the rhizosphere can strongly affect root health and development(7-9,11-18). Here, to understand how interactions between microorganisms influence root growth inArabidopsis, we established a model system for interactions between plants, microorganisms and the environment. We inoculated seedlings with a 185-member bacterial synthetic community, manipulated the abiotic environment and measured bacterial colonization of the plant. This enabled us to classify the synthetic community into four modules of co-occurring strains. We deconstructed the synthetic community on the basis of these modules, and identified interactions between microorganisms that determine root phenotype. These interactions primarily involve a single bacterial genus (Variovorax), which completely reverses the severe inhibition of root growth that is induced by a wide diversity of bacterial strains as well as by the entire 185-member community. We demonstrate thatVariovoraxmanipulates plant hormone levels to balance the effects of our ecologically realistic synthetic root community on root growth. We identify an auxin-degradation operon that is conserved in all available genomes ofVariovoraxand is necessary and sufficient for the reversion of root growth inhibition. Therefore, metabolic signal interference shapes bacteria-plant communication networks and is essential for maintaining the stereotypic developmental programme of the root. Optimizing the feedbacks that shape chemical interaction networks in the rhizosphere provides a promising ecological strategy for developing more resilient and productive crops.