Metabolite-driven fungal recruitment in rhizosphere explains superiority of organic fertilizer in enhancing the soil fertility of wheat

Abstract

Long-term application of conventional synthetic fertilizers (CF) significantly impairs soil fertility, particularly in the intensive wheat/maize rotation systems. The problem is even worse in medium-low yield farmlands such as lime concretion black soil, resulting in an inevitable threat to world's food security. Therefore, adopting innovative alternatives becomes an urgent need to improve soil fertility and fulfill agricultural high yield demands and sustainable development. Thus, we conducted a two-year field experiment in lime concretion black soil to compare the divergent effects of controlled-release (CRF), organic (OF) and microbial (MF) fertilizers on soil fertility improvement under wheat cultivation. Combined analysis using Linear discriminant analysis effect size, Orthogonal Partial Least Squares Discriminant Analysis, and Structural Equation Modeling revealed that CRF improved soil nitrogen retention via homocarnosine-mediated recruitment of the fungi Solicoccozyma aeria and Lecythophora. Specifically, CRF increased total nitrogen and alkali-hydrolyzable nitrogen by 17.3 % and 11.8 % compared to CF, respectively. Interestingly, OF demonstrated the most comprehensive improvement in soil fertility. OF enhanced multiple soil fertility by enriching Melatonin and Trioxilin A3, which facilitated the recruitment of Lophotrichus sp. and Lecythophora sp. This led to significant increases relative to CF in soil organic matter (18.3 %), total nitrogen (13.8 %), alkali-hydrolyzable nitrogen (10.0 %), available phosphorus (17.2 %), and available potassium (29.0 %). In contrast, MF promoted carbon accumulation by enriching melatonin and 3-hydroxycinnamic acid, recruiting Neocosmospora rubicola, which resulted in a 5.15 % increase in soil organic matter and an 11.4 % rise in microbial biomass carbon compared to CF. These findings demonstrate that novel fertilizers enhance soil fertility through metabolite-mediated recruitment of functional fungi rather than bacteria, with OF exhibiting the greatest synergistic effect between the rhizosphere metabolome and fungal assemblage. This study lays a theoretical foundation for tailored strategies that simultaneously enhance agricultural productivity and sustainability in lime concretion black soil regions under wheat/maize rotation systems.