Long-term compost fertilization enhanced soil disease suppressiveness by fostering interactions between root exudates and the rhizosphere microbiome

A detailed understanding of the interaction between agricultural management and the rhizosphere microbiome, particularly the role of root exudates, is crucial for leveraging the microbiome in sustainable agriculture. This study examined the influence of disease-suppressive soil, developed through long-term compost fertilization, on the root exudates of pepper plants, and how the elevated chemicals in these exudates affect the assembly of rhizosphere microbiome and the activity of Bacillus methylotrophicus 400 (BM400), a key antagonist against Phytophthora capsici. GC-TOF-MS analysis revealed a distinct composition of root exudates in the disease-suppressive soil, with significant enrichment of seven specific chemicals. A mini-rhizobox experiment demonstrated that a mixture of these seven enriched chemicals (MSEC) influenced the assembly of the rhizosphere microbiome, accounting for 11% of the variation in bacterial communities, and enriched in vitro antagonists against P. capsici, particularly in rhizosphere samples within 20 mm of the injection points. Most of the elevated chemicals attract BM400 and are utilized by it, enhancing its mobility. RNA-seq analysis further revealed that MSEC inhibited the transcription of genes related to protein synthesis and sporulation in BM400, while enhancing the expression of genes encoding urease. However, the impact of MSEC on microbiome assembly varied across the different soils from Shanghai, Guangdong, and Yancheng, and did not enhance BM400 survival. In conclusion, disease-suppressive soil altered the composition of root exudates, promoting the recruitment of beneficial microorganisms, though its effect on modifying the rhizosphere microbiome is highly context-dependent.