Hanbing Gao, Xiao He, Zhaohui Guo, Zhongliang Huang, Jaovola Ulrich Fernio, Xincheng Liu, Hangxi Liu, Qian Ge, Xuan Zhang, Jing Huang, Rui Xu
Effective land use in cadmium (Cd)-contaminated agricultural soils requires integrated strategies that not only promote phytoremediation but also enhance productivity and sustainability. However, whether these multifunctional goals can be simultaneously achieved through a rationally designed synthetic microbial community (SynCom) remains unclear. Here, this study developed a simplified plant–microbiome strategy that combines the perennial medicinal plant Artemisia argyi with a native rhizosphere SynCom to improve soil health, crop performance, and carbon sequestration. Field investigations initially showed that A. argyi cultivation enhanced soil Cd uptake by up to twofold and a threefold accumulation in soil organic matter. The custom high-throughput culturomics pipeline that enabled the identification and isolation efficiency of functional rhizobacteria from complex native communities (purity > 70 %). A top-down design strategy guided the assembly of a simplified, yet functionally complementary SynCom with minimal antagonism. The selected Pseudomonas–Rahnella pair exhibited strong Cd tolerance (∼ 2 mM), Plant growth promotion (PGP) traits, and carbon fixation capacity. SynCom inoculation under Cd stress confirmed stable endophytic colonization (10–15 %) rather than colonization of the rhizoplane, and significantly improved root biomass (+43 %), Cd uptake (+110 %), soil organic carbon accumulation (+50 %), and essential oil precursors. Rhizosphere and leaf metabolomics further indicated SynCom inoculation reallocated secondary metabolism supporting both plant’s resilience and oil biosynthesis. Our findings support a mechanistic model in which a simplified A. argyi + SynCom partnership enhances phytoremediation and productivity by coupling endophytic colonization, plant secondary metabolism, and microbial carbon turnover, thereby providing generalizable insights into how native SynCom can be rationally designed for multifunctional outcomes in contaminated soils.