Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant development
ABSTRACTPlant-associated diazotrophs strongly relate to plant nitrogen (N) supply and growth. However, our knowledge of diazotrophic community assembly and microbial N metabolism in plant microbiomes is largely limited. Here we examined the assembly and temporal dynamics of diazotrophic communities...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-04-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01055-23 |
| _version_ | 1797205210451410944 |
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| author | Chao Xiong Brajesh K. Singh Yong-Guan Zhu Hang-Wei Hu Pei-Pei Li Yan-Lai Han Li-Li Han Qin-Bing Zhang Jun-Tao Wang Si-Yi Liu Chuan-Fa Wu An-Hui Ge Li-Mei Zhang Ji-Zheng He |
| author_facet | Chao Xiong Brajesh K. Singh Yong-Guan Zhu Hang-Wei Hu Pei-Pei Li Yan-Lai Han Li-Li Han Qin-Bing Zhang Jun-Tao Wang Si-Yi Liu Chuan-Fa Wu An-Hui Ge Li-Mei Zhang Ji-Zheng He |
| author_sort | Chao Xiong |
| collection | DOAJ |
| description | ABSTRACTPlant-associated diazotrophs strongly relate to plant nitrogen (N) supply and growth. However, our knowledge of diazotrophic community assembly and microbial N metabolism in plant microbiomes is largely limited. Here we examined the assembly and temporal dynamics of diazotrophic communities across multiple compartments (soils, epiphytic and endophytic niches of root and leaf, and grain) of three cereal crops (maize, wheat, and barley) and identified the potential N-cycling pathways in phylloplane microbiomes. Our results demonstrated that the microbial species pool, influenced by site-specific environmental factors (e.g., edaphic factors), had a stronger effect than host selection (i.e., plant species and developmental stage) in shaping diazotrophic communities across the soil–plant continuum. Crop diazotrophic communities were dominated by a few taxa (~0.7% of diazotrophic phylotypes) which were mainly affiliated with Methylobacterium, Azospirillum, Bradyrhizobium, and Rhizobium. Furthermore, eight dominant taxa belonging to Azospirillum and Methylobacterium were identified as keystone diazotrophic taxa for three crops and were potentially associated with microbial network stability and crop yields. Metagenomic binning recovered 58 metagenome-assembled genomes (MAGs) from the phylloplane, and the majority of them were identified as novel species (37 MAGs) and harbored genes potentially related to multiple N metabolism processes (e.g., nitrate reduction). Notably, for the first time, a high-quality MAG harboring genes involved in the complete denitrification process was recovered in the phylloplane and showed high identity to Pseudomonas mendocina. Overall, these findings significantly expand our understanding of ecological drivers of crop diazotrophs and provide new insights into the potential microbial N metabolism in the phyllosphere.IMPORTANCEPlants harbor diverse nitrogen-fixing microorganisms (i.e., diazotrophic communities) in both belowground and aboveground tissues, which play a vital role in plant nitrogen supply and growth promotion. Understanding the assembly and temporal dynamics of crop diazotrophic communities is a prerequisite for harnessing them to promote plant growth. In this study, we show that the site-specific microbial species pool largely shapes the structure of diazotrophic communities in the leaves and roots of three cereal crops. We further identify keystone diazotrophic taxa in crop microbiomes and characterize potential microbial N metabolism pathways in the phyllosphere, which provides essential information for developing microbiome-based tools in future sustainable agricultural production. |
| first_indexed | 2024-04-24T08:47:30Z |
| format | Article |
| id | doaj.art-56b6ff4b8d1e4ca3a4d6182c26746ead |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-04-24T08:47:30Z |
| publishDate | 2024-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-56b6ff4b8d1e4ca3a4d6182c26746ead2024-04-16T13:00:55ZengAmerican Society for MicrobiologymSystems2379-50772024-04-019410.1128/msystems.01055-23Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant developmentChao Xiong0Brajesh K. Singh1Yong-Guan Zhu2Hang-Wei Hu3Pei-Pei Li4Yan-Lai Han5Li-Li Han6Qin-Bing Zhang7Jun-Tao Wang8Si-Yi Liu9Chuan-Fa Wu10An-Hui Ge11Li-Mei Zhang12Ji-Zheng He13State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaHawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, AustraliaState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaFaculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, AustraliaCollege of Resource and Environmental Sciences, Henan Agricultural University, Zhengzhou, ChinaCollege of Resource and Environmental Sciences, Henan Agricultural University, Zhengzhou, ChinaState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaSoil and Fertilizer Station of Qilin District, Qujing, Yunnan Province, ChinaHawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, AustraliaState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaABSTRACTPlant-associated diazotrophs strongly relate to plant nitrogen (N) supply and growth. However, our knowledge of diazotrophic community assembly and microbial N metabolism in plant microbiomes is largely limited. Here we examined the assembly and temporal dynamics of diazotrophic communities across multiple compartments (soils, epiphytic and endophytic niches of root and leaf, and grain) of three cereal crops (maize, wheat, and barley) and identified the potential N-cycling pathways in phylloplane microbiomes. Our results demonstrated that the microbial species pool, influenced by site-specific environmental factors (e.g., edaphic factors), had a stronger effect than host selection (i.e., plant species and developmental stage) in shaping diazotrophic communities across the soil–plant continuum. Crop diazotrophic communities were dominated by a few taxa (~0.7% of diazotrophic phylotypes) which were mainly affiliated with Methylobacterium, Azospirillum, Bradyrhizobium, and Rhizobium. Furthermore, eight dominant taxa belonging to Azospirillum and Methylobacterium were identified as keystone diazotrophic taxa for three crops and were potentially associated with microbial network stability and crop yields. Metagenomic binning recovered 58 metagenome-assembled genomes (MAGs) from the phylloplane, and the majority of them were identified as novel species (37 MAGs) and harbored genes potentially related to multiple N metabolism processes (e.g., nitrate reduction). Notably, for the first time, a high-quality MAG harboring genes involved in the complete denitrification process was recovered in the phylloplane and showed high identity to Pseudomonas mendocina. Overall, these findings significantly expand our understanding of ecological drivers of crop diazotrophs and provide new insights into the potential microbial N metabolism in the phyllosphere.IMPORTANCEPlants harbor diverse nitrogen-fixing microorganisms (i.e., diazotrophic communities) in both belowground and aboveground tissues, which play a vital role in plant nitrogen supply and growth promotion. Understanding the assembly and temporal dynamics of crop diazotrophic communities is a prerequisite for harnessing them to promote plant growth. In this study, we show that the site-specific microbial species pool largely shapes the structure of diazotrophic communities in the leaves and roots of three cereal crops. We further identify keystone diazotrophic taxa in crop microbiomes and characterize potential microbial N metabolism pathways in the phyllosphere, which provides essential information for developing microbiome-based tools in future sustainable agricultural production.https://journals.asm.org/doi/10.1128/msystems.01055-23plant microbiomediazotrophscereal cropsmicrobial networkssoil–plant continuumphyllosphere |
| spellingShingle | Chao Xiong Brajesh K. Singh Yong-Guan Zhu Hang-Wei Hu Pei-Pei Li Yan-Lai Han Li-Li Han Qin-Bing Zhang Jun-Tao Wang Si-Yi Liu Chuan-Fa Wu An-Hui Ge Li-Mei Zhang Ji-Zheng He Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant development mSystems plant microbiome diazotrophs cereal crops microbial networks soil–plant continuum phyllosphere |
| title | Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant development |
| title_full | Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant development |
| title_fullStr | Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant development |
| title_full_unstemmed | Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant development |
| title_short | Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant development |
| title_sort | microbial species pool mediated diazotrophic community assembly in crop microbiomes during plant development |
| topic | plant microbiome diazotrophs cereal crops microbial networks soil–plant continuum phyllosphere |
| url | https://journals.asm.org/doi/10.1128/msystems.01055-23 |
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