Maize-recruited Bacillus velezensis inhibit Fusarium oxysporum by directly secreting antimicrobial metabolites.

Abstract

Microorganisms of the crop rhizosphere are essential for maintaining crop health. Corn root rot (CRR) caused by Fusarium oxysporum is a severe disease that affects global maize yield and food security. Maize recruits beneficial rhizosphere microorganisms to resist F. oxysporum; however, the mechanism underlying this recruitment remains poorly understood. Here, we performed multi-omics analyses and experimental validation to investigate the microbial community in F. oxysporum-invaded maize roots. Maize-enriched Bacillus velezensis in the rhizosphere alleviated pathogenic stress by inhibiting F. oxysporum growth primarily through the direct production of antimicrobial metabolites that disrupted the pathogen's cellular structure. We elucidated the antimicrobial mechanism of the cell-free supernatant (CFS) by performing multi-omics analyses and validation. As CFS treatment duration increased, the pathogenic metabolic disorder intensified, and metabolic homeostasis of the genetic material showed increased disruption owing to interference of RNA processing and transcription. Additionally, the expression of pathogenicity-related genes NR1, STUA, and FOW was significantly downregulated. The key antimicrobial components comprised non-volatile metabolites (NVMs) of the benzenoid class (e.g., 4-Hydroxybenzaldehyde) and volatile metabolites (VOCs) of the alcohol and ketone classes (e.g., 5-methyl-2-heptanol) in the CFS. All compounds exhibited broad-spectrum antimicrobial activity. Thus, these results clarify the ecological strategy underlying the recruitment of beneficial B. velezensis in the rhizosphere of maize to resist F. oxysporum invasion, and they elucidate the specific antimicrobial mechanism of Bacillus. Notably, these findings provide an important foundation for future green prevention and control of soil-borne pathogens.