Mechanism, Regulation, and Ecology of Bacterial Auxin Degradation By the Genus Variovorax in the Complex Root Microbiome

Chemical signaling in the plant microbiome can have drastic effects on microbial community structure, and on host growth and development. Previously, we demonstrated that the auxin metabolic signal interference performed by the bacterial genus Variovorax via a novel auxin degradation locus was essential for maintaining stereotypic root development in an ecologically-relevant bacterial synthetic community. Here, we dissect the Variovorax auxin degradation locus to define the genes necessary and sufficient for indole-3-acetic acid (IAA) degradation and signal interference. We determine the crystal structures and binding properties of the locus’s MarR-family repressor with IAA and other auxins. We identify auxin-degradation loci across the bacterial tree of life and define two distinct types based on gene content and metabolic products: iac-like and Variovorax-like. We solve the structures of MarRs from representatives of each auxin degradation locus type, establishing that each have distinct IAA binding pockets. Comparison of representative IAA degrading strains from diverse bacterial genera show that while all degrade IAA, only strains containing a Variovorax-like auxin degradation locus interfere with auxin signaling in a complex synthetic community context. This suggests that Variovorax-like locus containing strains play a key ecological role in modulating auxins in the plant microbiome.