Metabolite-mediated microbial community modulation by Serratia marcescens enhances cucumber seedling growth in artificial cultivation systems

• Serratia marcescens LYGN1 enhances cucumber seedling vigor by 53.2–161 % , improving root activity, biomass, and nutrient uptake through elevated soil enzymatic activities (urease, phosphatase) and nutrient cycling. • LYGN1 reshapes substrate microbial communities , enriching beneficial genera ( Sphingopyxis, Serratia , rhizobia) and suppressing pathogens ( Ralstonia, Burkholderia ) via metabolite-mediated interactions. • Functional predictions reveal LYGN1-driven metabolic shifts , enhancing nitrogen/phosphorus metabolism, stress tolerance, and chlorophyll synthesis, critical for optimizing industrial seedling production systems. The application of plant growth-promoting rhizobacteria (PGPR) offers significant potential for enhancing crop productivity. Our previous study demonstrated Serratia marcescens LYGN1 could improve cucumber seedlings growth, though its mechanism remains incompletely understood. This study evaluated LYGN1 and its cell-free metabolites on cucumber seedlings in artificial substrates using four treatments: sterile water (CK), sterile medium (CM), bacterial suspension (TB), and cell-free filtrate (TF). Both TB and TF dramatically improved seedling performance, TF increased vigor index by 38.21 % and 100.15 % compared with CK at two sequential timepoints, while TB and TF elevated root vitality by 130.03 % and 110.12 %, respectively. Metabolite application comparably enhanced biomass, root architecture, and nutrient acquisition to that of live bacteria. Crucially, LYGN1 restructured the rhizosphere microbiome, enriching beneficial genera ( Sphingopyxis, Brevundimonas, Serratia ) and affect nitrogen/phosphorus metabolism via elevated enzyme activities. Metabolomic profiling identified auxin IAA and diverse bioactive compounds including alkaloids, organic acids in cell-free supernatant of LYGN1. These findings demonstrate that LYGN1-derived metabolites directly stimulate plant growth and indirectly optimize the rhizosphere microenvironment, positioning them as effective biostimulants for sustainable seedling production systems.