Core soil microbiota mediated by long-term organic fertilization enhance soil health and plant productivity

Soil health is essential for crop production and plays a crucial role in agricultural sustainability by supporting vital ecosystem and societal services. The manipulation of beneficial microbes is an emerging strategy for improving soil quality in agroecosystems. However, little is known about whether microbes enriched through organic fertilization can promote plant growth and soil health. This study employed amplicon sequencing and shotgun metagenomics to characterize the fertilizer-induced shifts in soil microbial communities and metabolism-related genes, and their correlations with soil health index. Core organic fertilizer-induced microbial taxa were then isolated and their growth-promoting and soil health-improving effects were experimentally verified. Our results demonstrated that the continuous application of organic fertilizer with higher nitrogen input enhanced soil health index by 119%. Random forest analyses revealed that the abundances of functional genes involved in nitrogen assimilation, especially nasB, gdh, and nirA were important predictors of soil health index. More importantly, functional genes involved in nitrogen cycling explained more variance (63.78%) in soil health index than phosphorus (38.73%) and carbon (32.33%) cycling. Furthermore, inoculation with synthetic communities (SynCom) derived from organic fertilization, which consisted of five Pseudomonas spp. and one Microbacterium sp., enhanced the soil health index by 36.1% compared to the non-inoculated control and significantly improved plant growth, including height, shoot dry weight, and root dry weight. These findings show that organic fertilization-induced core species enhance soil health and plant performance, laying the foundation for leveraging the beneficial microbes for sustainable agricultural practices.