Fumigation-driven restructuring of soil microbial ecosystems enhances endangered Fritillaria cirrhosa productivity and secondary metabolite biosynthesis: Insights from metabolomics and microbiome profiling

The intensive cultivation of Fritillaria cirrhosa, a critically endangered medicinal species, faces challenges due to continuous cropping obstacles (CCO) soil-borne pathogens and microecological imbalance. Although soil fumigation is an effective CCO mitigation strategy, the mechanistic linkages between fumigant-induced soil restructuring and enhancement of medicinal quality remain unresolved. In this study, we aimed to integrate microbiome-metabolomic analyses to systematically evaluate how four different fumigants modulate F. cirrhosa productivity, phytochemical biosynthesis, and soil ecological networks. Among the four fumigants evaluated, metam sodium (MS) the best performance as it increased the bulb biomass by 43.5 % relative to that of the control (CK), surpassing dazomet (21.11 %), dimethyl disulfide (1.62 %), and allyl isothiocyanate (9.77 %). MS treatment concurrently elevated medicinally critical metabolites, inducing 376.19 % and 12.90 % enhancement in cytidine and sipeimine contents, respectively. Soil analyses revealed MS-mediated nutrient activation, demonstrating a 10.70-fold increase in ammonium nitrogen and a 5.52-fold increase in available manganese compared with CK. Furthermore, MS selectively enriched beneficial plant growth-promoting rhizobacteria (Mesorhizobium, Pseudomonas, Paraburkholderia) while suppressing key phytopathogenic fungi, with the abundance of Cladosporium and Ilyonectria abundances decreasing 89.25 % and 96.64 % (P < 0.05), respectively. Metabolomic profiling indicated that all fumigants upregulated soil organic acids, lipids, and phospholipids. This enriched the metabolic pathways associated with microbial proliferation and soil restoration, including glycerophospholipid metabolism, aromatic compound degradation, and zeatin biosynthesis. Multivariate integration further demonstrated that defense-related metabolites (such as eriodictyol) exhibited strong positive correlations with nitrogen-fixing microbes, including Mycobacterium and Klebsiella (R > 0.50) but antagonistic relationships with Fusarium pathogens (R < −0.50). Collectively, our findings revealed that a mechanistic framework in which the fumigant-induced restructuring of soil microbial communities and metabolite-microbe synergism enhanced F. cirrhosa productivity and phytochemical quality. Our findings provide critical insights for addressing CCOs through precise soil management and offers practical strategies for the sustainable cultivation of endangered medicinal plants.