Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health
Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down con...
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| Published in | The ISME Journal Vol. 16; no. 8; pp. 1932 - 1943 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.08.2022
Oxford University Press |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in
Fusarium
wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g.
Bacillus
spp.). The pathogen-suppressive actions of predatory protists and
Bacillus
spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive
Bacillus
spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life. |
|---|---|
| AbstractList | Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life. Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life. Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life.Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life. |
| Author | Wang, Zhe Li, Rong Xiong, Wu Geisen, Stefan Tao, Chengyuan Xu, Zhihui Wang, Beibei Ruan, Yunze Shen, Qirong Guo, Sai Jousset, Alexandre Gao, Zhilei Liu, Shanshan Kowalchuk, George A. Shen, Zongzhuan |
| Author_xml | – sequence: 1 givenname: Sai surname: Guo fullname: Guo, Sai 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, Nanjing Agricultural University, Laboratory of Bio-interactions and Crop Health, Nanjing Agricultural University – sequence: 2 givenname: Chengyuan surname: Tao fullname: Tao, Chengyuan 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, Nanjing Agricultural University, Laboratory of Bio-interactions and Crop Health, Nanjing Agricultural University – sequence: 3 givenname: Alexandre surname: Jousset fullname: Jousset, Alexandre organization: Ecology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, Utrecht University – sequence: 4 givenname: Wu surname: Xiong fullname: Xiong, Wu 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, Nanjing Agricultural University, Laboratory of Bio-interactions and Crop Health, Nanjing Agricultural University, Ecology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, Utrecht University – sequence: 5 givenname: Zhe surname: Wang fullname: Wang, Zhe 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, Nanjing Agricultural University, Laboratory of Bio-interactions and Crop Health, Nanjing Agricultural University – sequence: 6 givenname: Zongzhuan surname: Shen fullname: Shen, Zongzhuan 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, Nanjing Agricultural University, Laboratory of Bio-interactions and Crop Health, Nanjing Agricultural University – sequence: 7 givenname: Beibei surname: Wang fullname: Wang, Beibei organization: Hainan Key Laboratory for Sustainable Utilization of Tropical Bio-resources, College of Tropical Crops, Hainan University – sequence: 8 givenname: Zhihui surname: Xu fullname: Xu, Zhihui 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, Nanjing Agricultural University, Laboratory of Bio-interactions and Crop Health, Nanjing Agricultural University – sequence: 9 givenname: Zhilei surname: Gao fullname: Gao, Zhilei organization: Ecology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, Utrecht University – sequence: 10 givenname: Shanshan surname: Liu fullname: Liu, Shanshan 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, Nanjing Agricultural University, Laboratory of Bio-interactions and Crop Health, Nanjing Agricultural University – sequence: 11 givenname: Rong orcidid: 0000-0002-2599-5476 surname: Li fullname: Li, Rong email: lirong@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, Nanjing Agricultural University, Laboratory of Bio-interactions and Crop Health, Nanjing Agricultural University – sequence: 12 givenname: Yunze surname: Ruan fullname: Ruan, Yunze organization: Hainan Key Laboratory for Sustainable Utilization of Tropical Bio-resources, College of Tropical Crops, Hainan University – sequence: 13 givenname: Qirong orcidid: 0000-0002-5662-9620 surname: Shen fullname: Shen, Qirong email: shenqirong@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, Nanjing Agricultural University, Laboratory of Bio-interactions and Crop Health, Nanjing Agricultural University – sequence: 14 givenname: George A. surname: Kowalchuk fullname: Kowalchuk, George A. organization: Ecology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, Utrecht University – sequence: 15 givenname: Stefan orcidid: 0000-0003-0734-727X surname: Geisen fullname: Geisen, Stefan organization: Laboratory of Nematology, Wageningen University, Netherlands Department of Terrestrial Ecology, Netherlands Institute for Ecology, (NIOO-KNAW) |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35461357$$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 2022 2022. The Author(s), under exclusive licence to International Society for Microbial Ecology. The Author(s), under exclusive licence to International Society for Microbial Ecology 2022. |
| Copyright_xml | – notice: The Author(s), under exclusive licence to International Society for Microbial Ecology 2022 – notice: 2022. 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 2022. |
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| DOI | 10.1038/s41396-022-01244-5 |
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| Title | Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health |
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