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.
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.
ISME J. 2023 Oct;17(10):1626-1638. doi: 10.1038/s41396-023-01476-z. Epub 2023 Jul 13.
Anthropogenic nitrogen inputs lead to a high ammonium (NH)/nitrate (NO) 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 NH-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 NH-enriched soil. Genetic manipulation, 16S rRNA gene analysis and coinoculation assays revealed that the genus Enterobacter was enriched in the hyphosphere of NH-sensitive wild-type compared to NH-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 NH:NO ratio following SZ2 inoculation. Microbial supplementation and inhibitor assays showed that AOA-mediated reduction in NH:NO ratio is responsible for SZ2-enhanced fungal adaptation to NH-enriched conditions. The Ph. liquidambaris-Enterobacter-AOA triple interaction promoted rice growth in NH-enriched soil. Our study reveals the essential role of hyphosphere microorganism-based hyphal spreading in plant-fungal symbiosis establishment within nitrogen-affected agroecosystems.
人为输入的氮会导致土壤中铵（NH）/硝酸盐（NO）的比例升高，从而限制土壤真菌的菌丝扩散。共生真菌进入根系是植物-真菌相互作用的前提。菌根细菌可以保护真菌免受环境压力的影响，但菌根细菌对宿主真菌适应富含 NH 的环境的影响尚不清楚。通过开发土壤微宇宙实验，我们报告称，植物共生真菌拟盘多毛孢（Phomopsis liquidambaris）拥有特定的菌根细菌，可以促进菌丝扩散，并有助于在富含 NH 的土壤中进行根系定殖。遗传操作、16S rRNA 基因分析和共接种实验表明，与 NH 偏好型亚硝酸盐还原酶缺陷菌株相比，在 NH 敏感型野生型的菌根中富集了肠杆菌属。代表性的肠杆菌属 SZ2 促进菌丝扩散仅在未灭菌的土壤中明显。我们进一步发现，在 SZ2 接种后，氨氧化古菌（AOA）的丰度和多样性增加，同时 NH：NO 比值降低。微生物补充和抑制剂实验表明，AOA 介导的 NH：NO 比值降低是 SZ2 增强真菌适应富含 NH 条件的原因。Ph. liquidambaris-Enterobacter-AOA 三重相互作用促进了 NH 丰富土壤中水稻的生长。我们的研究揭示了菌根微生物促进的菌丝扩散在受氮影响的农业生态系统中植物-真菌共生建立中的重要作用。
