Decoding endophytic microbiome dynamics: engineering antagonistic synthetic consortia for targeted fusarium suppression in monoculture regimes

Abstract

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.

Acknowledgements

The research was funded by the National Key Research and Development Program of China (2023YFD1900905; 2021YFD1901203), Hunan Science Fund for Distinguished Young Scholars (2022JJ10057), and the Natural Science Foundation of Hunan (2022JJ30647; 2022JJ30644).

Authors contributions

All authors made intellectual contributions and provided assistance to this study and manuscript. H.Q., L.Z., and B.Z. developed the initial framework. Z.R., C.F., F.H. assisted with field experiment maintenance and sampling. X.W., R.S., and A.T. conducted the cultivation of endophytes. Y.L., A.C., and P.L. contributed to the writing of the manuscript.

Data availability

The raw high-throughput sequence data of the bacterial 16S rRNA and fungal ITS genes have been deposited in the GenBank Sequence Read Archive under accession numbers PRJNA1155822 and PRJNA1155828, respectively. The raw sanger dideoxy sequence data of the bacterial 16S rRNA and fungal 18S rRNA genes reported in this paper were deposited in the GenBank under accession numbers PQ278707-PQ278760 and PQ276912-PQ276926, respectively.

Conflicts of interest statement

The authors declare that they have no conflict of interest.

Supplementary material

Supplementary material is available at Horticulture Research online.

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