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Decade-long fertilization and Bradyrhizobium inoculation reconfigure soybean rhizosphere microecology through fungal community assembly and metabolic niche partitioning

Wanling Wei1, 2, 3, Mingchao Ma1, Xin Jiang1, Fangang Meng4, Ping He1, 2, 3#, Jun Li1#

1 Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China 

2 Key Laboratory of Plant Nutrition and Fertiliser, Ministry of Agriculture and Rural Affairs, Beijing 100081, China 

3 State Key Laboratory of Efficient Utilisation of Arable Land in Northern China, Beijing 100081, China

4 Soybean Research Institute, Jilin Academy of Agricultural SciencesJilin 132011, China

 Highlights 

l Nitrogen fertilization initially reduces key antioxidant metabolite concentrations in soil.

Bradyrhizobium inoculation augments stress-related metabolite profiles at maturity.

Essential soil metabolites demonstrate correlation with fungal abundance and activity patterns.

l Pathway analysis identifies tryptophan and caffeine metabolism in stress response.

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摘要  

土壤微生物代谢物互作驱动作物生产力,然而其在豆科作物系统中对长期养分管理的响应机制仍需深入探究。本研究旨在阐明施肥与根瘤菌接种如何通过重构大豆根际真菌-代谢物互作网络以提升土壤健康。依托十年的田间试验,结合ITS测序和液相色谱-质谱联用(LC-MS)代谢组学技术,分析了四种处理:对照(CK)、磷钾肥(PK)、PK配施氮肥(PK+N、施PK肥并接种Bradyrhizobium japonicum 5821PK+R)。结果表明,施氮肥显著提高了成熟期真菌多样性并增强了共现网络复杂性(表现为最高的节点数和数),而接种慢生根瘤菌则提升了群落的随机性组装程度。土壤真菌与3-羟甲基安替比林(3-Hydroxymethylantipyrine)、大黄酚(Chrysophanol)、3,7-二羟基黄酮(3,7-Dihydroxyflavone)及三乙胺(Triethylamine)等代谢物呈现显著相关性。代谢谱分析进一步揭示:施氮肥抑制了抗胁迫黄酮类化合物(3-羟甲基安替比林、大黄酚、3,7-二羟基黄酮)的积累,而接种慢生根瘤菌显著富集这些关键代谢物。KEGG通路富集分析证实,在开花结荚期,色氨酸代谢和咖啡因代谢是协调氮素同化与防御响应的核心通路。此外,上述关键代谢物的丰度与土壤全氮、有机质及碱解氮含量显著相关。本研究证实,接种慢生根瘤菌可与施肥协同作用激活真菌群落驱动的关键代谢途径,为大豆体系提供基于微生物组的增效减投(提升氮素利用率减少化肥投入)策略。



Abstract  

Soil microbial-metabolite interactions influence crop productivity, yet their responses to long-term nutrient management in legume systems warrant further investigation. This study examined how fertilization and Rhizobium inoculation reshape soybean rhizosphere fungal-metabolite networks to improve soil health. Through a decade-long field trial utilizing Internal Transcribed Spacer (ITS) sequencing and Liquid Chromatography-Mass Spectrometry (LC-MS) metabolomics, four treatments were evaluated: control (CK), phosphorus-potassium fertilization (PK), PK with nitrogen fertilization (PK+N), and PK with Bradyrhizobiumjaponicum 5821 inoculation (PK+R). Results indicated that nitrogen fertilization increased fungal diversity at maturity and enhanced co-occurrence network complexity (displaying the highest node and edge counts), while Bradyrhizobium inoculation promoted stochastic assembly. Soil fungi exhibited notable correlations with 3-Hydroxymethylantipyrine, Chrysophanol, 3,7-Dihydroxyflavone and Triethylamine. Metabolite profiling revealed nitrogen suppression of stress-resistance flavonoids (3-Hydroxymethylantipyrine, Chrysophanol, 3,7-Dihydroxyflavone), whereas Bradyrhizobium enhanced these key metabolites. KEGG enrichment identified tryptophan and caffeine metabolism as central during flowering-podding, coordinating nitrogen assimilation and defense responses. Additionally, the key metabolites correlated significantly with soil total nitrogen, organic matter, and available nitrogen. These findings reveal that Bradyrhizobium acts synergistically with fertilization to activate fungal-driven metabolic pathways, offering a microbiome-based approach to enhance nitrogen efficiency and reduce agrochemical dependency in soybean systems.

Keywords:  fungal community       key differential metabolites       Rhizobium       soil microecology  
Online: 07 July 2025  
Fund: 

This work was supported by the National Key Technology Research and Development Program of China (2023YFD1702200), the National Natural Science Foundation of China (42373080), the Major Science and Technology Project of Yunnan Province, China (202202AE090025) and the Earmarked Fund for China Agriculture Research System (CARS-04).

About author:  Wanling Wei, E-mail: weiwanlingwwl@163.com; #Correspondence Ping He, E-mail: heping02@caas.cn; Jun Li, E-mail: lijun01@caas.cn

Cite this article: 

Wanling Wei, Mingchao Ma, Xin Jiang, Fangang Meng, Ping He, Jun Li. 2025. Decade-long fertilization and Bradyrhizobium inoculation reconfigure soybean rhizosphere microecology through fungal community assembly and metabolic niche partitioning. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.07.010

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