Plant-derived benzoxazinoids act as antibiotics and shape bacterial communities

Plants synthesize and release specialized metabolites into their environment that can serve as chemical cues for other organisms. Metabolites that are released from the roots are important factors in determining which microorganisms will colonize the root and become part of the plant rhizosphere. Root exudates can be converted by soil microorganisms, which can result in the formation of toxic compounds. How individual members of the plant rhizosphere respond to individual compounds and how the differential response of individual microorganisms contributes to the response of a microbial community remains an open question. Here, we investigated the impact of derivatives of benzoxazinoids, a class of plant root exudates released by important crops such as wheat and maize, on a collection of 180 root-associated bacteria. Phenoxazine, derived in soil from benzoxazinoids, inhibited the growth of root-associated bacteria in vitro in an isolate-specific manner, with sensitive and resistant isolates present in most of the studied clades. Using synthetic communities, we show that community stability is a consequence of the resilience of its individual members, with communities assembled from tolerant isolates being overall more tolerant to benzoxazinoids. However, the performance of an isolate in a community context was not correlated with its individual performance but appeared to be shaped by interactions between isolates. These interactions were independent of the overall community composition and were strain-specific, with interactions between different representatives of the same bacterial genera accounting for differential community composition.