Rhizosphere metabolite-mediated soil enhancement: long-term biochar application optimizes continuous soybean production systems

Abstract Biochar offers promising solutions for agricultural sustainability, yet the intricate mechanisms governing rhizosphere metabolite-microbe-soil interactions remain poorly understood. Through a decade-long field experiment, the effects of sustained biochar application (BC1: 3 t ha −1 and BC2: 6 t ha −1 ) versus conventional fertilization (CF) in a continuous soybean system were investigated. The results showed that biochar improved soil properties, especially, BC2, which significantly enhanced porosity (+ 12.71%), pH (+ 11.60%), soil organic carbon (+ 112.45%), enzymatic activities and nutrient content, while reducing bulk density (− 9.92%). Notably, the biochar restructured microbial community networks, increasing beneficial taxa (Firmicutes, Enterococcus , Pseudomonas, Ascomycota and Mortierellomycota) while suppressing potential pathogens. Meanwhile, the biochar significantly optimized rhizosphere metabolites, including key defensive compounds (di-O-methyl quercetin, capric acid, hypoxanthines, etc.), and optimized the differential metabolites enriched in the isoflavonoid biosynthesis pathway. Multi-omics analysis revealed strong correlations between differential metabolites and improved soil properties under biochar amendment. Accordingly, these improvements manifested in plant performance, including enhanced root development, plant height, biomass accumulation, and yield. Furthermore, the PLS-PM analysis demonstrated that biochar could promote soybean growth in two key pathway mechanisms that directly enhance soil properties, and indirectly improve soil properties by negatively regulating the key metabolites (capric acid, phosphocreatine, beta 1-tomatine, and daidzin). Our findings provide critical theoretical insights for addressing challenges in soybean continuous cropping systems and advancing sustainable farming practices. Graphical Abstract