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 Trichoderma harzianum T19 and five Bacillus strains and tested it in nonsterile soil challenged with Fusarium pseudograminearum. 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 Fusarium in the rhizosphere and enriched beneficial microbes, including antagonistic fungi (Trichoderma, Chaetomium) and plant growth-promoting bacteria (Pseudomonas, Paenibacillus). 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 F. pseudograminearum 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.