Microbiota-mediated nitrogen fixation and microhabitat homeostasis in aerial root-mucilage
Abstract Background Plants sustain intimate relationships with diverse microbes. It is well-recognized that these plant-associated microbiota shape individual performance and fitness of host plants, but much remains to be explored regarding how they exert their function and maintain their homeostasi...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-04-01
|
| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01525-x |
| _version_ | 1797840900507828224 |
|---|---|
| author | Zhiqiang Pang Xinyu Mao Shaoqun Zhou Sheng Yu Guizhou Liu Chengkai Lu Jinpeng Wan Lingfei Hu Peng Xu |
| author_facet | Zhiqiang Pang Xinyu Mao Shaoqun Zhou Sheng Yu Guizhou Liu Chengkai Lu Jinpeng Wan Lingfei Hu Peng Xu |
| author_sort | Zhiqiang Pang |
| collection | DOAJ |
| description | Abstract Background Plants sustain intimate relationships with diverse microbes. It is well-recognized that these plant-associated microbiota shape individual performance and fitness of host plants, but much remains to be explored regarding how they exert their function and maintain their homeostasis. Results Here, using pink lady (Heterotis rotundifolia) as a study plant, we investigated the phenomenon of microbiota-mediated nitrogen fixation and elucidated how this process is steadily maintained in the root mucilage microhabitat. Metabolite and microbiota profiling showed that the aerial root mucilage is enriched in carbohydrates and diazotrophic bacteria. Nitrogen isotope-labeling experiments, 15N natural abundance, and gene expression analysis indicated that the aerial root-mucilage microbiota could fix atmospheric nitrogen to support plant growth. While the aerial root mucilage is a hotspot of nutrients, we did not observe high abundance of other environmental and pathogenic microbes inside. We further identified a fungus isolate in mucilage that has shown broad-spectrum antimicrobial activities, but solely allows the growth of diazotrophic bacteria. This “friendly” fungus may be the key driver to maintain nitrogen fixation function in the mucilage microhabitat. Video Abstract Conclusion The discovery of new biological function and mucilage-habitat friendly fungi provides insights into microbial homeostasis maintenance of microenvironmental function and rhizosphere ecology. |
| first_indexed | 2024-04-09T16:22:23Z |
| format | Article |
| id | doaj.art-0fa3972eb1cc49cb947c86aeceece8e6 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-09T16:22:23Z |
| publishDate | 2023-04-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-0fa3972eb1cc49cb947c86aeceece8e62023-04-23T11:23:39ZengBMCMicrobiome2049-26182023-04-0111111710.1186/s40168-023-01525-xMicrobiota-mediated nitrogen fixation and microhabitat homeostasis in aerial root-mucilageZhiqiang Pang0Xinyu Mao1Shaoqun Zhou2Sheng Yu3Guizhou Liu4Chengkai Lu5Jinpeng Wan6Lingfei Hu7Peng Xu8CAS Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of SciencesCAS Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of SciencesShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural SciencesShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural SciencesCAS Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of SciencesCAS Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of SciencesCAS Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of SciencesInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang UniversityCAS Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of SciencesAbstract Background Plants sustain intimate relationships with diverse microbes. It is well-recognized that these plant-associated microbiota shape individual performance and fitness of host plants, but much remains to be explored regarding how they exert their function and maintain their homeostasis. Results Here, using pink lady (Heterotis rotundifolia) as a study plant, we investigated the phenomenon of microbiota-mediated nitrogen fixation and elucidated how this process is steadily maintained in the root mucilage microhabitat. Metabolite and microbiota profiling showed that the aerial root mucilage is enriched in carbohydrates and diazotrophic bacteria. Nitrogen isotope-labeling experiments, 15N natural abundance, and gene expression analysis indicated that the aerial root-mucilage microbiota could fix atmospheric nitrogen to support plant growth. While the aerial root mucilage is a hotspot of nutrients, we did not observe high abundance of other environmental and pathogenic microbes inside. We further identified a fungus isolate in mucilage that has shown broad-spectrum antimicrobial activities, but solely allows the growth of diazotrophic bacteria. This “friendly” fungus may be the key driver to maintain nitrogen fixation function in the mucilage microhabitat. Video Abstract Conclusion The discovery of new biological function and mucilage-habitat friendly fungi provides insights into microbial homeostasis maintenance of microenvironmental function and rhizosphere ecology.https://doi.org/10.1186/s40168-023-01525-xRhizosphere ecologyMucilage microhabitatDiazotrophFriendly microbeMicrobial homeostasis |
| spellingShingle | Zhiqiang Pang Xinyu Mao Shaoqun Zhou Sheng Yu Guizhou Liu Chengkai Lu Jinpeng Wan Lingfei Hu Peng Xu Microbiota-mediated nitrogen fixation and microhabitat homeostasis in aerial root-mucilage Microbiome Rhizosphere ecology Mucilage microhabitat Diazotroph Friendly microbe Microbial homeostasis |
| title | Microbiota-mediated nitrogen fixation and microhabitat homeostasis in aerial root-mucilage |
| title_full | Microbiota-mediated nitrogen fixation and microhabitat homeostasis in aerial root-mucilage |
| title_fullStr | Microbiota-mediated nitrogen fixation and microhabitat homeostasis in aerial root-mucilage |
| title_full_unstemmed | Microbiota-mediated nitrogen fixation and microhabitat homeostasis in aerial root-mucilage |
| title_short | Microbiota-mediated nitrogen fixation and microhabitat homeostasis in aerial root-mucilage |
| title_sort | microbiota mediated nitrogen fixation and microhabitat homeostasis in aerial root mucilage |
| topic | Rhizosphere ecology Mucilage microhabitat Diazotroph Friendly microbe Microbial homeostasis |
| url | https://doi.org/10.1186/s40168-023-01525-x |
| work_keys_str_mv | AT zhiqiangpang microbiotamediatednitrogenfixationandmicrohabitathomeostasisinaerialrootmucilage AT xinyumao microbiotamediatednitrogenfixationandmicrohabitathomeostasisinaerialrootmucilage AT shaoqunzhou microbiotamediatednitrogenfixationandmicrohabitathomeostasisinaerialrootmucilage AT shengyu microbiotamediatednitrogenfixationandmicrohabitathomeostasisinaerialrootmucilage AT guizhouliu microbiotamediatednitrogenfixationandmicrohabitathomeostasisinaerialrootmucilage AT chengkailu microbiotamediatednitrogenfixationandmicrohabitathomeostasisinaerialrootmucilage AT jinpengwan microbiotamediatednitrogenfixationandmicrohabitathomeostasisinaerialrootmucilage AT lingfeihu microbiotamediatednitrogenfixationandmicrohabitathomeostasisinaerialrootmucilage AT pengxu microbiotamediatednitrogenfixationandmicrohabitathomeostasisinaerialrootmucilage |