Temporal microbiome succession across plant-nematode niches drives soybean cyst nematode suppression

Abstract Background Soybean cyst nematode (SCN; Heterodera glycines ) is one of the most destructive pathogens of soybean worldwide. Current management strategies rely on a limited set of resistant soybean varieties, crop rotation, and chemical nematicides that are increasingly constrained by breakdown of host resistance and growing environmental concerns. Although accumulating evidence suggests that continuous cropping can develop SCN-suppressive soils, the microbial and ecological processes driving their formation remain poorly understood. Results In this study, we established SCN-suppressive soils by successively planting SCN-susceptible soybean in SCN-infested soil under controlled conditions and transferring rhizosphere microbiomes from each preceding planting cycle. Successive plantings significantly reduced SCN egg densities, which stabilized at low levels in later cycles. Microbial profiling of SCN cyst, root endosphere, and rhizosphere revealed substantial restructuring across planting cycles, with rhizosphere showing the greatest differentiation. Bacterial alpha diversity was negatively correlated with SCN egg densities, whereas fungal diversity showed positive correlations. Core microbiome analysis detected no core bacterial taxa consistently shared across compartments or planting cycles, but several core fungal taxa persisted. Differential abundance analyses revealed compartment-specific functional shifts: early planting cycles were characterized by higher abundance of taxa previously reported to be associated with plant nutrient acquisition or pathogenicity, including Bradyrhizobium , Microlunatus , Setophoma , Ustilago , Fusarium , Dactylonectria , and members of Nectriaceae, whereas later cycles showed enrichment of taxa with putative antagonistic activity, such as Ohtaekwangia , Streptomyces , Pseudomonas , and members of Bacillales. Association analyses further demonstrated compartment-specific correlations with SCN egg density: microbial taxa positively correlated with SCN were enriched in early cycles but declined over cycles, whereas negatively correlated taxa accumulated in later cycles, reflecting consistent temporal dynamics across compartments. Culture-based screening identified several potential nematicidal bacteria, with Bacillus sp. (B34) consistently suppressing SCN in susceptible soybean. Conclusions This study demonstrated that successive soybean monoculture under SCN pressure could drive the formation of SCN-suppressive soils through coordinated, compartment-specific microbial succession. SCN population decline was associated with a shift from early-cycle communities enriched in taxa previously reported to be associated with nutrient acquisition or pathogenicity to later-cycle communities enriched in microbes with antagonistic potential. These findings highlighted the critical roles of host- and nematode- associated microbiome assembly and spatiotemporal dynamics in natural disease suppression and supported microbiome-based strategy for sustainable SCN management.