Bacillus velezensis stimulates resident rhizosphere Pseudomonas stutzeri for plant health through metabolic interactions
Trophic interactions play a central role in driving microbial community assembly and function. In gut or soil ecosystems, successful inoculants are always facilitated by efficient colonization; however, the metabolite exchanges between inoculants and resident bacteria are rarely studied, particularl...
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| Published in | The ISME Journal Vol. 16; no. 3; pp. 774 - 787 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.03.2022
Oxford University Press |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Trophic interactions play a central role in driving microbial community assembly and function. In gut or soil ecosystems, successful inoculants are always facilitated by efficient colonization; however, the metabolite exchanges between inoculants and resident bacteria are rarely studied, particularly in the rhizosphere. Here, we used bioinformatic, genetic, transcriptomic, and metabonomic analyses to uncover syntrophic cooperation between inoculant (
Bacillus velezensis
SQR9) and plant-beneficial indigenous
Pseudomonas stutzeri
in the cucumber rhizosphere. We found that the synergistic interaction of these two species is highly environmental dependent, the emergence of syntrophic cooperation was only evident in a static nutrient-rich niche, such as pellicle biofilm in addition to the rhizosphere. Our results identified branched-chain amino acids (BCAAs) biosynthesis pathways are involved in syntrophic cooperation. Genome-scale metabolic modeling and metabolic profiling also demonstrated metabolic facilitation among the bacterial strains. In addition, biofilm matrix components from
Bacillus
were essential for the interaction. Importantly, the two-species consortium promoted plant growth and helped plants alleviate salt stress. In summary, we propose a mechanism in which synergic interactions between a biocontrol bacterium and a partner species promote plant health. |
|---|---|
| AbstractList | Trophic interactions play a central role in driving microbial community assembly and function. In gut or soil ecosystems, successful inoculants are always facilitated by efficient colonization; however, the metabolite exchanges between inoculants and resident bacteria are rarely studied, particularly in the rhizosphere. Here, we used bioinformatic, genetic, transcriptomic, and metabonomic analyses to uncover syntrophic cooperation between inoculant (
Bacillus velezensis
SQR9) and plant-beneficial indigenous
Pseudomonas stutzeri
in the cucumber rhizosphere. We found that the synergistic interaction of these two species is highly environmental dependent, the emergence of syntrophic cooperation was only evident in a static nutrient-rich niche, such as pellicle biofilm in addition to the rhizosphere. Our results identified branched-chain amino acids (BCAAs) biosynthesis pathways are involved in syntrophic cooperation. Genome-scale metabolic modeling and metabolic profiling also demonstrated metabolic facilitation among the bacterial strains. In addition, biofilm matrix components from
Bacillus
were essential for the interaction. Importantly, the two-species consortium promoted plant growth and helped plants alleviate salt stress. In summary, we propose a mechanism in which synergic interactions between a biocontrol bacterium and a partner species promote plant health. Trophic interactions play a central role in driving microbial community assembly and function. In gut or soil ecosystems, successful inoculants are always facilitated by efficient colonization; however, the metabolite exchanges between inoculants and resident bacteria are rarely studied, particularly in the rhizosphere. Here, we used bioinformatic, genetic, transcriptomic, and metabonomic analyses to uncover syntrophic cooperation between inoculant (Bacillus velezensis SQR9) and plant-beneficial indigenous Pseudomonas stutzeri in the cucumber rhizosphere. We found that the synergistic interaction of these two species is highly environmental dependent, the emergence of syntrophic cooperation was only evident in a static nutrient-rich niche, such as pellicle biofilm in addition to the rhizosphere. Our results identified branched-chain amino acids (BCAAs) biosynthesis pathways are involved in syntrophic cooperation. Genome-scale metabolic modeling and metabolic profiling also demonstrated metabolic facilitation among the bacterial strains. In addition, biofilm matrix components from Bacillus were essential for the interaction. Importantly, the two-species consortium promoted plant growth and helped plants alleviate salt stress. In summary, we propose a mechanism in which synergic interactions between a biocontrol bacterium and a partner species promote plant health. Trophic interactions play a central role in driving microbial community assembly and function. In gut or soil ecosystems, successful inoculants are always facilitated by efficient colonization; however, the metabolite exchanges between inoculants and resident bacteria are rarely studied, particularly in the rhizosphere. Here, we used bioinformatic, genetic, transcriptomic, and metabonomic analyses to uncover syntrophic cooperation between inoculant (Bacillus velezensis SQR9) and plant-beneficial indigenous Pseudomonas stutzeri in the cucumber rhizosphere. We found that the synergistic interaction of these two species is highly environmental dependent, the emergence of syntrophic cooperation was only evident in a static nutrient-rich niche, such as pellicle biofilm in addition to the rhizosphere. Our results identified branched-chain amino acids (BCAAs) biosynthesis pathways are involved in syntrophic cooperation. Genome-scale metabolic modeling and metabolic profiling also demonstrated metabolic facilitation among the bacterial strains. In addition, biofilm matrix components from Bacillus were essential for the interaction. Importantly, the two-species consortium promoted plant growth and helped plants alleviate salt stress. In summary, we propose a mechanism in which synergic interactions between a biocontrol bacterium and a partner species promote plant health.Trophic interactions play a central role in driving microbial community assembly and function. In gut or soil ecosystems, successful inoculants are always facilitated by efficient colonization; however, the metabolite exchanges between inoculants and resident bacteria are rarely studied, particularly in the rhizosphere. Here, we used bioinformatic, genetic, transcriptomic, and metabonomic analyses to uncover syntrophic cooperation between inoculant (Bacillus velezensis SQR9) and plant-beneficial indigenous Pseudomonas stutzeri in the cucumber rhizosphere. We found that the synergistic interaction of these two species is highly environmental dependent, the emergence of syntrophic cooperation was only evident in a static nutrient-rich niche, such as pellicle biofilm in addition to the rhizosphere. Our results identified branched-chain amino acids (BCAAs) biosynthesis pathways are involved in syntrophic cooperation. Genome-scale metabolic modeling and metabolic profiling also demonstrated metabolic facilitation among the bacterial strains. In addition, biofilm matrix components from Bacillus were essential for the interaction. Importantly, the two-species consortium promoted plant growth and helped plants alleviate salt stress. In summary, we propose a mechanism in which synergic interactions between a biocontrol bacterium and a partner species promote plant health. |
| Author | Xie, Jiyu Strube, Mikael L. Kovács, Ákos T. Shen, Qirong Sun, Xinli Zheng, Daoyue Xu, Zhihui Tan, Taimeng Zhang, Ruifu Hesselberg-Thomsen, Viktor Dragoš, Anna |
| Author_xml | – sequence: 1 givenname: Xinli surname: Sun fullname: Sun, Xinli organization: Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Bacterial Interactions and Evolution Group, DTU Bioengineering, Technical University of Denmark – sequence: 2 givenname: Zhihui orcidid: 0000-0002-3987-8836 surname: Xu fullname: Xu, Zhihui email: xzh2068@njau.edu.cn organization: Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, The Key Laboratory of Plant Immunity, Nanjing Agricultural University – sequence: 3 givenname: Jiyu surname: Xie fullname: Xie, Jiyu organization: Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, The Key Laboratory of Plant Immunity, Nanjing Agricultural University – sequence: 4 givenname: Viktor orcidid: 0000-0001-6929-3671 surname: Hesselberg-Thomsen fullname: Hesselberg-Thomsen, Viktor organization: Bacterial Interactions and Evolution Group, DTU Bioengineering, Technical University of Denmark, Bacterial Ecophysiology and Biotechnology Group, DTU Bioengineering, Technical University of Denmark, Quantitative Modelling of Cell Metabolism Group, The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark – sequence: 5 givenname: Taimeng surname: Tan fullname: Tan, Taimeng organization: Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, The Key Laboratory of Plant Immunity, Nanjing Agricultural University – sequence: 6 givenname: Daoyue surname: Zheng fullname: Zheng, Daoyue organization: Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, The Key Laboratory of Plant Immunity, Nanjing Agricultural University – sequence: 7 givenname: Mikael L. orcidid: 0000-0003-0905-5705 surname: Strube fullname: Strube, Mikael L. organization: Bacterial Ecophysiology and Biotechnology Group, DTU Bioengineering, Technical University of Denmark – sequence: 8 givenname: Anna orcidid: 0000-0003-4136-986X surname: Dragoš fullname: Dragoš, Anna organization: Bacterial Interactions and Evolution Group, DTU Bioengineering, Technical University of Denmark, Biotechnical Faculty, University of Ljubljana – sequence: 9 givenname: Qirong orcidid: 0000-0002-5662-9620 surname: Shen fullname: Shen, Qirong organization: Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, The Key Laboratory of Plant Immunity, Nanjing Agricultural University – sequence: 10 givenname: Ruifu orcidid: 0000-0002-3334-4286 surname: Zhang fullname: Zhang, Ruifu email: rfzhang@njau.edu.cn organization: Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, The Key Laboratory of Plant Immunity, Nanjing Agricultural University – sequence: 11 givenname: Ákos T. orcidid: 0000-0002-4465-1636 surname: Kovács fullname: Kovács, Ákos T. organization: Bacterial Interactions and Evolution Group, DTU Bioengineering, Technical University of Denmark |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34593997$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author(s), under exclusive licence to International Society for Microbial Ecology 2021 2021. The Author(s), under exclusive licence to International Society for Microbial Ecology. The Author(s), under exclusive licence to International Society for Microbial Ecology 2021. |
| Copyright_xml | – notice: The Author(s), under exclusive licence to International Society for Microbial Ecology 2021 – notice: 2021. The Author(s), under exclusive licence to International Society for Microbial Ecology. – notice: The Author(s), under exclusive licence to International Society for Microbial Ecology 2021. |
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| GrantInformation_xml | – fundername: National Natural Science Foundation of China (National Science Foundation of China) grantid: 32072675; 32072665 funderid: https://doi.org/10.13039/501100001809 – fundername: Danmarks Grundforskningsfond (Danish National Research Foundation) grantid: DNRF137 funderid: https://doi.org/10.13039/501100001732 – fundername: National Nature Science Foundation of China 31972512 – fundername: National Nature Science Foundation of China (31972512, 32072675 and 32072665), the Agricultural Science and Technology Innovation Program of CAAS (CAAS-ZDRW202009), the Fundamental Research Funds for the Central Universities (KYXK202009). XS was supported by a Chinese Scholarship Council fellowship. ÁTK, MLS and AD were supported by the Danish National Research Foundation (DNRF137) for the Center for Microbial Secondary Metabolites. AD was supported by Slovenian Research Agency (N1-0177). Biofilm related work in the group of ÁTK is supported by a DTU Alliance Strategic Partnership PhD fellowship. Funding from Novo Nordisk Foundation (grant NNFOC0055625) for the infrastructure “Imaging microbial language in biocontrol (IMLiB)” is acknowledged. – fundername: Novo Nordisk Fonden (Novo Nordisk Foundation) grantid: NNFOC0055625 funderid: https://doi.org/10.13039/501100009708 – fundername: ; – fundername: ; grantid: DNRF137 – fundername: ; grantid: NNFOC0055625 – fundername: ; grantid: 32072675; 32072665 |
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| Title | Bacillus velezensis stimulates resident rhizosphere Pseudomonas stutzeri for plant health through metabolic interactions |
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