Biological control leveraging endophytic microbes represents a promising eco-friendly strategy to mitigate soil-borne diseases, yet the efficacy and mechanistic underpinnings of synthetic microbial communities (SynComs) derived from plant endophytes remain poorly understood. This study employed a holistic approach—integrating field sampling, microbial profiling, and functional validation—to investigate the dynamics of edible lily (Lilium) microbiomes under continuous cropping and develop targeted SynComs against Fusarium oxysporum. Metacommunity analysis revealed that prolonged monoculture co-enriched both potentially beneficial taxa (e.g. Pseudomonas, Bacillus) and pathogenic Fusarium, reflecting a dynamic equilibrium where naturally recruited antagonists were insufficient to prevent pathogen dominance, while increasing the complexity of endophytic co-occurrence networks. Keystone bacterial lineages, including Burkholderiaceae and Pseudomonas, emerged as critical stabilizers of the endosphere microbiome. Notably, 50% of endogenous bacterial taxa exhibited rhizospheric origins, contrasting with fungal communities where <10% derived from soil—a finding underscoring host-specific filtering mechanisms. Through systematic isolation and combinatorial testing, we engineered SynComs combining core antagonistic strains (Rhizobium, Methylobacterium, Talaromyces) with auxiliary microbes. Fungal-integrated SynComs outperformed bacteria-only consortia in plant growth promotion and pathogen suppression. By bridging fundamental microbial ecology with translational agriculture, our findings establish SynComs as scalable tools for sustainable soil health management, reducing reliance on synthetic fungicides while addressing the yield-limiting challenges in continuous cropping systems.

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