Narrow-spectrum resource-utilizing bacteria drive the stability of synthetic communities through enhancing metabolic interactions

The importance of synthetic microbial communities in agriculture is increasingly being recognized, but methods for constructing targeted synthetic communities using existing microbial resources remain limited. In this study, six plant beneficial bacterial strains with distinct capacities for utilizing rhizosphere resources and functions of nitrogen fixation, phosphate solubilization, indoleacetic acid synthesis, and siderophore production were selected to construct stable and multifunctional communities for promoting plant growth. Metabolic modeling revealed a negative correlation between resource utilization width and community stability: that is, narrow-spectrum resource-utilizing strains enhanced metabolic interaction potential and reduced metabolic resource overlap, thereby increasing the stability of the community. Comprehensive validation, including large-scale simulations, metabolite supplementation, cross-feeding, and in situ experiments, consistently confirmed the central roles of the narrow-spectrum resource-utilizing strains, Cellulosimicrobium cellulans E and Pseudomonas stutzeri G, which formed metabolic interaction networks via the secretion of asparagine, vitamin B12, isoleucine, and their precursors or derivatives. Two synthetic multifunctional communities, SynCom4 and SynCom5, demonstrated high stability in the tomato rhizosphere and led to an increase in plant dry weight by over 80%. Our study elucidates the link between resource utilization width and community stability, providing a rational basis for the construction of stable, multifunctional microbial communities for specific habitats.