Long-term continuous cropping reshapes soybean rhizosphere microbiome and metabolome to alleviate allelopathic stress and enhance disease suppression

BACKGROUND: Continuous cropping obstacles (CCO) pose a persistent threat to global soybean sustainability, yet paradoxically attenuate under prolonged monoculture. To explore this, we investigated the soil-plant-microbiome dynamics across 1-year, short-term continuous cropping (STCC, 7-13 years), and long-term continuous cropping (LTCC, 19-25 years) systems. RESULTS: Our results reveal that LTCC reduces the accumulation of allelopathic autotoxin by 49.06% (P < 0.05) and enriches beneficial rhizosphere metabolites (e.g., antibiotics, monoterpenes, and glycoside compounds), driving a shift in the microbial community towards taxa with pathogen-suppressive and nutrient-cycling functions. LTCC cultivated a microbiome with enhanced genes for stress resistance and nutrient uptake. Conversely, STCC exacerbates CCO stress, with microbial dysbiosis peaking at 13 years (Simpson index down 15.4%). Notably, 25-year LTCC restores ecosystem stability and enzyme activity, restructuring microbial communities with pathogen-suppressive and nutrient-cycling functions. By reintroducing depleted taxa including Pseudomonas, Burkholderia, and Enterobacter spp., we constructed a synthetic community, SC7. SC7 boosted soil enzymes and root nodules to shield plants from stress, increasing yield by 4.83% and mimicking long-term system advantages. CONCLUSIONS: This study demonstrates the self-repair capacity of soybean monoculture. It bridges the gap between mechanistic insights, specifically the microbiome-metabolite feedback, and actionable solutions, such as SC7 inoculation. As a result, it advances sustainable intensification strategies for global soybean production. Video Abstract.