Silica Nanoparticles Drive Disease-Suppressive Microbiome Assembly Via Inosine-Associated Metabolic Reprogramming and Biofilm Promotion

Soil metabolites serve as critical cues that orchestrate the assembly of microbial communities. However, the precise mechanisms by which specific chemical signals mediate plant–microbiome interactions to enhance disease resistance remain elusive. In particular, how engineered nanomaterials, such as SiO2 NPs, leverage this metabolic signaling to promote the establishment of disease-suppressive microbiomes is largely unexplored. We integrated metagenomics, metabolomics, and transcriptomics to elucidate the synergy between SiO2 NP–driven soil metabolic reprogramming and the establishment of biocontrol bacteria. We first demonstrated that SiO2 NPs inhibited potato common scab in a dose-dependent manner and drove significant shifts in soil microbial community structure and network complexity. We identified Bacillus as a core SiO2 NP–responsive taxon, and experiments showed that Bacillus velezensis strain PH3-11 inhibited pathogenic Streptomyces, with isovaleric acid emerging as a candidate antimicrobial metabolite associated with this antagonistic activity. Metabolomic and metagenomic analyses further indicated that SiO2 NPs stimulated inosine accumulation, and inosine was strongly associated with the community structure of SiO2 NP-responsive biomarkers. Mechanistically, transcriptomic analysis showed that inosine, as a SiO2 NP–responsive metabolite, upregulated genes involved in extracellular polysaccharide synthesis in strain PH3-11 (e.g., epsD, epsN, and epsO) and markedly promoted biofilm formation by PH3-11. Field trials further confirmed a synergistic effect of co-applying inosine with strain PH3-11, which was superior to single-strain inoculation in promoting biocontrol bacterial colonization, suppressing disease, and enhancing soil microbiome stability. Our findings unveil a “nano-metabolite-microbiome” cascade, suggesting that SiO2 NPs promote the enrichment of protective biofilm-forming bacteria by reprogramming the soil metabolome and promoting inosine accumulation. This study supports an inosine-associated mechanism contributing to disease-suppressive microbiome assembly and highlights the potential of nano-enabled synbiotics to manipulate chemical–biological coupling for sustainable plant health.