Integrated the rhizosphere soil microbiota and metabolome reveal mechanisms inhibiting Phytophthora nicotianae under long-term bio-organic fertilizer application

• Long-term bio-organic fertilizer application altered soil organic matter and urease levels. • Long-term bio-organic fertilizer application altered soil microbial communities. • Long-term bio-organic fertilizer application significantly altered soil metabolites. • The change of soil fertility, microorganisms and metabolites together enhance crop health. Rational bio-organic fertilizer application has important advantages in reducing chemical fertilizer application, mitigating environmental pollution risks and enhancing plant health. However, the interplay between rhizosphere soil microbial communities, associated metabolites and the inhibiting pathogenic bacteria mechanisms is required, particularly in the long-term bio-organic fertilizer application. Therefore, our study encompassed three experimental conditions: conventional chemical fertilizer application (CF), 20 % reduction in chemical fertilizer supplemented with organic fertilizer (OF) and 20 % chemical fertilizer reduction supplemented with bio-organic fertilizer (BOF). By integrating microbiology and metabonomics, we aimed to elucidate the effects of long-term different fertilizer measures on the rhizosphere soil microbial community and metabolic function. Compared with CF, the relative abundance of Phytophthora nicotianae in rhizosphere soil and corresponding disease significantly decreased with BOF. However, there were significant increases in the concentrations of nitrate nitrogen, total nitrogen, available phosphorus, organic matter and urease activity. Simultaneously, the relative abundance of Proteobacteria at the phylum level notably increased with BOF, whereas the relative abundance of Gemmatimonas and Sphingomonas at the genus level exhibited significant increases. Moreover, the BOF affected the complexity and stability of the soil bacterial symbiotic networks. Furthermore, the metabolite profiles were significantly altered, with the differential metabolites in KEGG metabolic pathways being notably enriched for BOF treatment, particularly in pathways related to gibberellin secondary metabolite, histidine, and tryptophan metabolism. The correlation analysis and structural equation modeling revealed significant interactions between soil properties, microorganisms and metabolites, all of which had a substantial impact on the disease incidence. Consequently, we observed that soil fertility, rhizosphere microorganisms and tryptophan metabolites collectively facilitated the favorable response of crop health to the partial replacement of chemical fertilizers with bio-organic alternatives. These findings provided novel insights into sustainable practices of the reduction of chemical fertilizer and environmental pollution.