Synthetic communities of maize root bacteria interact and redirect benzoxazinoid metabolization

Plant roots are colonized by diverse microbial communities. These communities are shaped by root exudates, including plant-specialized metabolites. Benzoxazinoids are such secreted compounds of maize. Individual microbes differ in their ability to tolerate and metabolize antimicrobial benzoxazinoids. To investigate how these traits combine in a community, we designed two synthetic communities of maize root bacteria that share six common strains and differ in their ability to metabolize benzoxazinoids based on the seventh strain. We exposed both communities to the benzoxazinoid MBOA (6-methoxybenzoxazolin-2(3H)-one) in vitro and found that the metabolizing community did not degrade MBOA to its aminophenoxazinone, as observed for individual strains, but, as a community, they formed the corresponding acetamide. MBOA shaped the differential compositions of both communities and increased the fraction of MBOA-tolerant strains. The benzoxazinoid-metabolizing community showed a higher tolerance to MBOA and was able to utilize MBOA as their sole carbon source for growth. Hence, bacterial interaction results in alternative benzoxazinoid metabolization and increases community performance in the presence of these antimicrobial compounds. Future work is needed to uncover the genetics of this metabolic interaction and ecological consequences for the bacterial community and the host plant.IMPORTANCEWe investigated how maize root bacteria-alone or in community-tolerate and metabolize antimicrobial compounds of their host plant. We found that the capacity to metabolize such a compound impacts bacterial community size and structure and, most importantly, benefits community fitness. We also found that interacting bacteria redirected the metabolization of the antimicrobial compound to an alternative degradation pathway. Our work highlights the need to study the teamwork of microbes to uncover their community traits to ultimately understand the ecological consequences for the bacterial community and eventually the host plant.