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Hyphosphere microorganisms facilitate hyphal spreading and root colonization of plant symbiotic fungus in ammonium-enriched soil

The ISME Journal volume 17, pages 1626–1638 (2023)Cite this article

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Abstract

Anthropogenic nitrogen inputs lead to a high ammonium (NH4+)/nitrate (NO3−) ratio in the soil, which restricts hyphal spreading of soil fungi. Access of symbiotic fungi to roots is a prerequisite for plant-fungal interactions. Hyphosphere bacteria protect fungi from environmental stress, yet the impact of hyphosphere bacteria on adaptation of host fungi to NH4+-enriched conditions remains unclear. By developing soil microcosm assays, we report that a plant-symbiotic fungus, Phomopsis liquidambaris, harbors specific hyphosphere bacteria that facilitate hyphal spreading and assist in the root colonization in NH4+-enriched soil. Genetic manipulation, 16S rRNA gene analysis and coinoculation assays revealed that the genus Enterobacter was enriched in the hyphosphere of NH4+-sensitive wild-type compared to NH4+-preferring nitrite reductase‐deficient strain. The representative Enterobacter sp. SZ2-promoted hyphal spreading is only evident in nonsterilized soil. We further identified an increased abundance and diversity of ammonia-oxidizing archaea (AOA) and a synchronously decreased NH4+:NO3− ratio following SZ2 inoculation. Microbial supplementation and inhibitor assays showed that AOA-mediated reduction in NH4+:NO3− ratio is responsible for SZ2-enhanced fungal adaptation to NH4+-enriched conditions. The Ph. liquidambaris-Enterobacter-AOA triple interaction promoted rice growth in NH4+-enriched soil. Our study reveals the essential role of hyphosphere microorganism-based hyphal spreading in plant-fungal symbiosis establishment within nitrogen-affected agroecosystems.

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Fig. 1: Soil microorganisms assist Ph. liquidambaris in spreading to the rhizosphere of rice and root colonization under NH4+-enriched conditions.
Fig. 2: The Enterobacter bacteria are enriched in NH4+-sensitive WT hyphosphere but depleted in the NH4+-preferring Δnir hyphosphere under NH4+-enriched conditions.
Fig. 3: Analysis of Ph. liquidambaris-Enterobacter sp. SZ2 interaction.
Fig. 4: Enterobacter sp. SZ2 enhances Ph. liquidambaris adaption to NH4+-enriched condition by reducing hyphosphere NH4+:NO3− ratio.
Fig. 5: Ammonia oxidizing archaea (AOA) are attracted by Enterobacter sp. SZ2 and synchronously involved in SZ2-reduced NH4+:NO3− ratio in the hyphosphere of Ph. liquidambaris.
Fig. 6: Enterobacter bacteria establish multiple interactive relationships with saprotrophic fungi with differential responses to NH4+-enriched condition.
Fig. 7: Ph. liquidambaris-Enterobacter coinoculation increases ammonia oxidizing archaea (AOA) abundance in the rice rhizosphere and promotes plant growth.
Fig. 8: A model illustrating the fungal-Enterobacter interaction facilitating hyphae of Ph. liquidambaris spreading to the rhizosphere of rice under NH4+-enriched conditions.

Data availability

Supplementary methods, figures, tables and results are provided in the file Supplementary Information. The 16S rRNA and amoAF/amoAR gene sequencing data are available in the NCBI SRA under BioProject PRJNA835591 and PRJNA837065, respectively.

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Acknowledgements

We would like to acknowledge the National Natural Science Foundation of China (No. 32071638), Jiangsu Funding Program for Excellent and Postdoctoral Talent (2022ZB357), China Postdoctoral Science Foundation (2021M701748), and a project funded by the Priority Academic Program Development (PAPD) of the Jiangsu Higher Education Institutions of China.

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  1. Jiangsu Key Laboratory for Microbes and Functional Genomics, Jiangsu Engineering and Technology Research Center for Industrialization of Microbial Resources, College of Life Sciences, Nanjing Normal University, Nanjing, Jiangsu Province, China

    Kai Sun, Hui-Jun Jiang, Yi-Tong Pan, Fan Lu, Qiang Zhu, Chen-Yu Ma, Ai-Yue Zhang, Wei Zhang & Chuan-Chao Dai

  2. Jiangsu Key Laboratory for the Research and Uti1ization of Plant Resources, Jiangsu Provincial Platform for Conservation and Utilization of Agricultural Germplasm, Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, Jiangsu, China

    Jia-Yu Zhou

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KS, WZ, and CCD designed the study and wrote the manuscript. KS, HJJ, YTP, and FL performed experiments. KS, QZ, CYM, and AYZ analyzed the data. JYZ revised the paper. All of authors read and approved the final manuscript.

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Sun, K., Jiang, HJ., Pan, YT. et al. Hyphosphere microorganisms facilitate hyphal spreading and root colonization of plant symbiotic fungus in ammonium-enriched soil. ISME J 17, 1626–1638 (2023). https://doi.org/10.1038/s41396-023-01476-z

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