Metabolic analysis of a bacterial synthetic community from maize roots provides new mechanistic insights into microbiome stability

Stability is a desirable property for agricultural microbiomes, but there is a poor understanding of the mechanisms that mediate microbial community stability. Recently, a representative bacterial synthetic community from maize roots has been proposed as a model system to study microbiome stability (Niu 2017, PNAS, 114:E2450). This SynCom assembles stably when all seven members are present, but community diversity collapses without the keystone E. cloacae strain. The aim of this study was to assess the role of metabolites for the stability of this SynCom, by defining the metabolic niches occupied by each strain, as well as their cross-feeding phenotypes and B-vitamin dependencies. We show that the individual member strains occupy complementary metabolic niches, measured by the depletion of distinct metabolites in exometabolomic experiments, as well as contrasting growth phenotypes on diverse carbon substrates. Minimal medium experiments show that the established seven-member community comprises a mixture of prototrophic and auxotrophic strains. Correspondingly, experimental cross-feeding phenotypes showed that spent media harvested from the prototrophic strains can sustain growth of two auxotrophs. We suggest that the metabolic mechanisms exhibited by this SynCom could serve as design principles to inform the rational assembly of stable plant-associated microbial communities.