Phyllosphere microbiota and metabolomic insights of sewage sludge-derived biostimulant in enhancing nutritional quality and disease resistance of Pakchoi cabbage

• SS-NB increased biomass and nutritional quality through foliar and soil fertilization. • SS-NB enhances photosynthetic efficiency by activating the Rubisco enzyme and ATP synthase. • SS-NB(SF) is more conducive to the production of phytohormone analogues. • SS-NB(FF) improves disease resistance through phyllosphere bacteria-metabolite positive interactions. • SS-NB(SF) inhibits phyllosphere pathogens via flavonoid metabolites in a negative interaction mode. Maintaining green and sustainable agriculture is challenging due to the reliance on chemical fertilizers and pesticides. Sewage sludge-based nutrient biostimulant (SS-NB), derived from alkaline thermal hydrolysis of sludge, offers both nutrient and biostimulant properties, making it a promising alternative. However, its effect on the physiological characteristics of crops remains unclear. In this study, we explored changes in the growth characteristics, metabolic molecules, and phyllosphere microbial communities of pakchoi cabbage following both foliar fertilization (FF) and soil fertilization (SF) with SS-NB. Both SS-NB(FF) and SS-NB(SF) treatments increased the net photosynthetic rate, light energy use efficiency, ATP synthase, and Rubisco enzyme activities in the photosynthesis system. The related metabolites were mainly involved in carbon fixation, sugar metabolism, amino acid metabolism, and disease-resistant metabolic pathways. In addition, SS-NB(SF) significantly enhanced the abundance of phytohormone analogues, which had strong positive correlations with photosynthesis and nutrient metabolites (up to 60.81%). Meanwhile, SS-NB(FF) and SS-NB(SF) reduced the crop's dependence on phyllosphere photosynthetic microorganisms and elevated the abundance of phyllosphere beneficial microorganisms. In the SS-NB(FF) group, bacteria acted as a hub for nutrient transformation and maintained strong interaction with metabolites, which in turn enhanced the disease resistance of the crop. Conversely, the SS-NB(SF) group suppressed phyllosphere pathogens through flavonoids in a negative interaction mode. Overall, SS-NB may enhance crop growth and disease resistance by inducing the production of phytohormonal substances and stimulating photosynthesis, nutrient metabolism, and flavonoid metabolic pathways. This study provides data support for SS-NB as a nutrient input to enhance sustainable agricultural production.