Long‐Term Inorganic Nitrogen Fertilization Drives a Trade‐Off in the Soybean Symbiotic Network From Low‐Loss Fixation to High‐Loss Metabolism

Abstract

The productivity and sustainability of legume crops are highly dependent on their tripartite symbiotic system with rhizobia and arbuscular mycorrhizal fungi (AMF), a system currently facing significant pressure from long‐term excessive nitrogen (N) fertilization. However, how long‐term N input and host niche selection jointly regulate the structure and function of this tripartite symbiotic system remains poorly understood. Using a soybean pot experiment with soils collected in 2022 from a 24‐year field experiment (winter wheat–summer maize rotation, receiving annual urea at 0, 200, 400, 600 kg N ha −1 year −1 since 1998), we systematically elucidated these mechanisms. The results demonstrate that host niche selection is the dominant driver structuring the core symbiotic network. This manifests as a progressive, stringent homogeneous selection for rhizobia from soil to nodules, and as dispersal limitation for AMF, imposed by strong physical filtration at the root epidermis. Long‐term N input nonlinearly disrupted this host‐dominated framework. Specifically, excessive N fertilization shifted rhizobial community assembly from deterministic to stochastic dominance, weakened their cross‐kingdom synergy with AMF, and triggered a transition in the systemic N‐cycling pathway. This transition moved from an efficient, low‐loss internal symbiotic N‐fixation mode to a high‐loss‐risk external N metabolism mode. This functional trade‐off ultimately compromised the system's nutrient accumulation and retention capacity, offering a mechanistic explanation for how excessive N fertilization drives agroecosystems from symbiosis‐dependence to fertilizer‐dependence. These findings demonstrate that optimizing N management sustains nutrient retention and productivity by preserving the host‐shaped symbiotic network, offering a reference for reducing fertilizer dependence and improving the sustainability of legume production.

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