Suppressive microbiome protects against mulberry wilt by safeguarding host glycosylphosphatidylinositol-anchor biosynthesis.

AIMS: Soil-borne pathogens pose a significant threat to global agriculture. While certain soils naturally suppress disease, the complex interplay between different microbial kingdoms and their metabolic functions in orchestrating this suppression remains poorly understood.

METHODS AND RESULTS: We integrated 16S/ITS/18S rRNA amplicon sequencing with nontargeted liquid chromatography-tandem mass spectrometry (LC-MS/MS) metabolomics to elucidate the multikingdom microbial drivers and metabolic profiles of rhizosphere soils from healthy (HS) and diseased (DS) mulberry (Morus alba L.) orchards. The HS orchard, under long-term organic fertilization, exhibited strong disease suppression (12% incidence), whereas the DS orchard, under chemical fertilization, was highly susceptible (85% incidence) to wilt disease. The HS soils harbored a more complex and stable microbial co-occurrence network. This community was significantly enriched in putative beneficial taxa, including the bacteria Stenotrophomonas and Pseudomonas, the fungus Mortierella, and the predatory protist Colpoda. In contrast, the pathogen Fusarium was enriched in DS soils. Functional profiling predicted that the HS microbiome possessed a higher potential for antibiotic biosynthesis and stress tolerance. Metabolomic analysis revealed a striking divergence in metabolic pathways. DS plants mounted a massive but ineffective defense, characterized by the accumulation of phytoalexins. We identified a significant downregulation of the glycosylphosphatidylinositol-anchor biosynthesis pathway in DS soils, a fundamental process for anchoring functional proteins to the plant cell surface.

CONCLUSIONS: Our findings reveal a novel pathogenic strategy of targeting host cell-surface architecture and the corresponding community-level defense mechanism.