Metabolic rewiring and transcriptional interference underlie the biocontrol efficacy of Burkholderia arboris BB417 against Ralstonia solanacearum species complex.

Ralstonia solanacearum species complex (RSSC) is a globally destructive plant pathogen with high ecological persistence, making bacterial wilt management a long-standing challenge. In this study, we identified Burkholderia arboris BB417 as a potent biocontrol agent and systematically elucidated its multilevel antagonistic mechanisms against RSSC. BB417 exhibited broad-spectrum inhibition against diverse RSSC strains and achieved greenhouse control efficacy comparable to chemical pesticides within the 10-day observation period, while also promoting plant growth through nitrogen fixation, phosphate solubilization, and indole-3-acetic acid production. Genomic, transcriptomic and metabolomic analyses revealed that BB417 imposed strong nutrient competition and antimicrobial pressure, triggering extensive metabolic reprogramming in RSSC. The pathogen responded by upregulating motility-related genes as an avoidance strategy, while simultaneously experiencing disruptions in nitrogen metabolism, sulfur metabolism, membrane integrity, and energy homeostasis. L-glutamate emerged as a central metabolic and signaling node, integrating ABC transporters, two-component systems, and nitrogen-energy coupling pathways. Its depletion by the biocontrol bacterium BB417 redirected RSSC-resources from virulence toward stress defense. Conversely, exogenous supplementation of L-glutamate enhanced RSSC resistance to BB417, further validating a pivotal role of L-glutamate in mediating the biocontrol bacterium-pathogen interaction. Overall, this study provides mechanistic insights into pathogen-biocontrol interactions and highlights BB417 as a promising resource for sustainable bacterial wilt management.