Root exudates enhance the ecological fitness of a non-native PGPR and reshape rhizosphere microbiome assembly

Abstract

Root exudates play critical roles in rhizosphere microbiome assembly. Nevertheless, the molecular mechanisms by which plant growth-promoting rhizobacteria (PGPR) perceive these signals, adapt to the rhizosphere, and influence native microbial communities remain poorly understood. Here, using maize (Zea mays cv. Early Golden Bantam) and the rhizobacterium Priestia aryabhattai AB211, we took a multi-omics approach combining metabolomics, bacterial transcriptomics and proteomics, and rhizosphere metagenomics to elucidate the mechanism underlying this process. Maize root exudates were enriched in diverse carbon and nitrogen metabolites that promoted bacterial growth and induced extensive molecular reprogramming of pathways involved in nutrient acquisition, chemotaxis, motility, stress adaptation, and plant growth promotion, thereby enhancing rhizosphere competence. In field-conditioned soil, AB211 persisted as a core member of the maize rhizosphere microbiome, promoted early seedling growth, and reshaped microbial community composition and function. Root exudates-primed (RE-primed) AB211 further enhanced the enrichment of microbial functions associated with nutrient cycling, quorum sensing, plant growth promotion, and rhizosphere fitness, highlighting the role of root exudates in modulating the rhizosphere-adaptative potential of beneficial bacteria. These findings establish a mechanistic framework linking root exudates composition with PGPR adaptation and microbiome assembly, providing a foundation for engineering ecologically adapted microbial inoculants to improve crop productivity and sustainable agriculture.