Cross-Kingdom Synthetic Microbiota Suppresses Wheat Fusarium Crown Rot by Remodeling the Rhizosphere Microbiome and Metabolome

Fusarium crown rot (FCR) of wheat lacks sustainable control. We assembled a cross-kingdom synthetic microbial community (SMC) of <i>Trichoderma harzianum</i> T19 and five <i>Bacillus</i> strains and tested it in nonsterile soil challenged with <i>Fusarium pseudograminearum</i>. The SMC treatment significantly suppressed FCR, reducing the disease severity index by approximately 70%. Wheat growth and yield were simultaneously enhanced. In the rhizosphere, SMC improved soil health by elevating soil organic matter and nitrogen levels by over 50%, while mitigating pathogen-induced nutrient imbalances and boosting nutrient-cycling enzyme activities. Amplicon sequencing revealed that SMC suppressed pathogenic <i>Fusarium</i> in the rhizosphere and enriched beneficial microbes, including antagonistic fungi (<i>Trichoderma</i>, <i>Chaetomium</i>) and plant growth-promoting bacteria (<i>Pseudomonas</i>, <i>Paenibacillus</i>). Co-occurrence network analysis showed that SMC treatment restructured the rhizosphere microbial network with higher connectivity, stability, and a prevalence of positive cooperative interactions under <i>F. pseudograminearum</i> stress. Defense-related metabolites, such as epi-jasmonic acid, allantoin, Nβ-acetyltryptamine, and dihydrodaidzein, accumulated to higher levels with SMC. These findings demonstrate that the cross-kingdom SMC modulates soil nutrients, microbial community structure, and rhizosphere metabolites to synergistically promote wheat growth and enhance resistance to FCR.