Triple-coupling of genomic potential, metabolite diversity, and microbial community optimization drives Bacillus velezensis DH18-mediated resistance to Fusarium root rot and growth promotion in strawberry

ABSTRACT Fusarium oxysporum -induced root rot severely threatens strawberry production, necessitating effective mitigation strategies. Beneficial microorganisms that simultaneously suppress disease and promote plant growth offer promising solutions, yet their multiscale mechanisms remain poorly understood. Here, a dual-functional strain, Bacillus velezensis DH18, exhibiting both plant growth-promoting and disease-suppressive activities, was isolated from the rhizosphere of strawberry plants affected by root rot. Strain DH18 exhibited remarkable effectiveness against strawberry root rot, achieving disease control efficacies of 86.95% and 89.49% in pot and field experiments, respectively. Concurrently, the strain significantly promoted strawberry plant growth and enhanced nutrient content in both the rhizosphere soil and leaves. Whole-genome sequencing revealed that DH18 possesses numerous biosynthetic gene clusters (BGCs) linked to antimicrobial metabolite production, alongside genes involved in plant growth-promoting traits. Metabolite profiling further identified key bioactive compounds, such as surfactin, salicylic acid, and citric acid, which are correlated with disease suppression and growth promotion. Moreover, microbial community analysis demonstrated that DH18 application reshaped the rhizosphere community by enriching beneficial genera (e.g., Bacillus , Pseudomonas , and Mortierella ), while suppressing the phytopathogen Fusarium , thereby contributing to a disease-suppressive soil environment. These findings suggest that the disease suppression and plant growth promotion conferred by B. velezensis DH18 are associated with an integrated mechanism involving its genomic potential, metabolite diversity, and beneficial modulation of the soil microbial community.‌ This work not only positions DH18 as a promising dual-functional bioinoculant but also provides insights into the molecular and ecological bases of plant growth-promoting rhizobacteria (PGPR)-mediated benefits. IMPORTANCE Strawberry production faces severe challenges from Fusarium root rot, which threatens crop yields and sustainability. Chemical controls often harm ecosystems, highlighting the need for eco-friendly alternatives. This study introduces Bacillus velezensis DH18, a beneficial ‌bacterium that combats root rot while boosting plant growth. Field tests show it reduces disease by over 85% and enhances soil health. DH18 works through multiple pathways: producing natural compounds like surfactin to inhibit pathogens, enriching helpful microbes in the soil, and improving nutrient uptake. These findings offer a safe, effective solution to replace synthetic chemicals, promoting sustainable agriculture. By understanding how DH18 integrates genomic, metabolic, and microbial community actions, the research advances the use of biological inoculants for healthier crops and environments.