Precision Probiotics in Agroecosystems: Multiple Strategies of Native Soil Microbiotas for Conquering the Competitor Ralstonia solanacearum
ABSTRACT Ralstonia solanacearum (Rs), a soilborne phytopathogen, causes bacterial wilt disease in a broad range of hosts. Common approaches, for example, the direct reduction of the pathogen using classic single broad-spectrum probiotics, suffer from poor colonization efficiency, interference by res...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-06-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01159-21 |
| _version_ | 1818545529168068608 |
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| author | Jiakang Yin Ziliang Zhang Yixiong Guo Yue Chen Yang Xu Wenxuan Chen Yanan Shao Youfeng Yu Lixia Zhu Lingling Chen Lifang Ruan |
| author_facet | Jiakang Yin Ziliang Zhang Yixiong Guo Yue Chen Yang Xu Wenxuan Chen Yanan Shao Youfeng Yu Lixia Zhu Lingling Chen Lifang Ruan |
| author_sort | Jiakang Yin |
| collection | DOAJ |
| description | ABSTRACT Ralstonia solanacearum (Rs), a soilborne phytopathogen, causes bacterial wilt disease in a broad range of hosts. Common approaches, for example, the direct reduction of the pathogen using classic single broad-spectrum probiotics, suffer from poor colonization efficiency, interference by resident microbiota, and nonnative-microorganism invasion. The soil microbiota plays an important role in plant health. Revealing the intrinsic linkage between the microbiome and the occurrence of disease and then applying it to agroecosystems for the precise control of soilborne diseases should be an effective strategy. Here, we surveyed the differences in the microbiome between healthy and diseased soils used for tomato planting across six climatic regions in China by using 16S rRNA amplicon and metagenomic sequencing. The roles of species associated with disease symptoms were further validated. Healthy soil possessed more diverse bacterial communities and more potential plant probiotics than diseased soil. Healthy soil simultaneously presented multiple strategies, including specifically antagonizing Rs, decreasing the gene expression of the type III secretion system of Rs, and competing for nutrition with Rs. Bacteria enriched in diseased samples promoted the progression of tomato bacterial wilt by strengthening the chemotaxis of pathogens. Therefore, Rs and its collaborators should be jointly combatted for disease suppression. Our research provides integrated insights into a multifaceted strategy for the biocontrol of tomato bacterial wilt based on the individual network of local microbiota. IMPORTANCE In the current work, the relationship between the soil microbiota and tomato bacterial wilt on a large scale offered us a comprehensive understanding of the disease. The delicate strategy of the microbiota in soil used for growing tomatoes to conquer the strong competitor, Rs, was revealed by microbiome research. The collaborators of Rs that coexist in a common niche with Rs strengthened our understanding of the pathogenesis of bacterial wilt. Bacteria enriched in healthy soil that antagonized pathogens with high specificity provide a novel view for ecofriendly probiotics mining. Our study offers new perspectives on soilborne-pathogen biocontrol in agroecosystems by decoding the rule of the natural ecosystem. |
| first_indexed | 2024-12-12T07:41:21Z |
| format | Article |
| id | doaj.art-88343f5f93dc4b72b705f674d56c0a13 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-12T07:41:21Z |
| publishDate | 2022-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-88343f5f93dc4b72b705f674d56c0a132022-12-22T00:32:46ZengAmerican Society for MicrobiologymSystems2379-50772022-06-017310.1128/msystems.01159-21Precision Probiotics in Agroecosystems: Multiple Strategies of Native Soil Microbiotas for Conquering the Competitor Ralstonia solanacearumJiakang Yin0Ziliang Zhang1Yixiong Guo2Yue Chen3Yang Xu4Wenxuan Chen5Yanan Shao6Youfeng Yu7Lixia Zhu8Lingling Chen9Lifang Ruan10State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaState Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaNational Key Laboratory of Crop Genetic Improvement, College of Informatics, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaState Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaCollege of Humanities and Social Sciences, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaCollege of Humanities and Social Sciences, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaState Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaState Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaThe Academy of Agriculture and Forestry Science of Panzhihua City, Panzhihua, People’s Republic of ChinaNational Key Laboratory of Crop Genetic Improvement, College of Informatics, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaState Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, People’s Republic of ChinaABSTRACT Ralstonia solanacearum (Rs), a soilborne phytopathogen, causes bacterial wilt disease in a broad range of hosts. Common approaches, for example, the direct reduction of the pathogen using classic single broad-spectrum probiotics, suffer from poor colonization efficiency, interference by resident microbiota, and nonnative-microorganism invasion. The soil microbiota plays an important role in plant health. Revealing the intrinsic linkage between the microbiome and the occurrence of disease and then applying it to agroecosystems for the precise control of soilborne diseases should be an effective strategy. Here, we surveyed the differences in the microbiome between healthy and diseased soils used for tomato planting across six climatic regions in China by using 16S rRNA amplicon and metagenomic sequencing. The roles of species associated with disease symptoms were further validated. Healthy soil possessed more diverse bacterial communities and more potential plant probiotics than diseased soil. Healthy soil simultaneously presented multiple strategies, including specifically antagonizing Rs, decreasing the gene expression of the type III secretion system of Rs, and competing for nutrition with Rs. Bacteria enriched in diseased samples promoted the progression of tomato bacterial wilt by strengthening the chemotaxis of pathogens. Therefore, Rs and its collaborators should be jointly combatted for disease suppression. Our research provides integrated insights into a multifaceted strategy for the biocontrol of tomato bacterial wilt based on the individual network of local microbiota. IMPORTANCE In the current work, the relationship between the soil microbiota and tomato bacterial wilt on a large scale offered us a comprehensive understanding of the disease. The delicate strategy of the microbiota in soil used for growing tomatoes to conquer the strong competitor, Rs, was revealed by microbiome research. The collaborators of Rs that coexist in a common niche with Rs strengthened our understanding of the pathogenesis of bacterial wilt. Bacteria enriched in healthy soil that antagonized pathogens with high specificity provide a novel view for ecofriendly probiotics mining. Our study offers new perspectives on soilborne-pathogen biocontrol in agroecosystems by decoding the rule of the natural ecosystem.https://journals.asm.org/doi/10.1128/msystems.01159-21soil microbiomeRalstonia solanacearumprecision probioticsmultifaceted biocontrol |
| spellingShingle | Jiakang Yin Ziliang Zhang Yixiong Guo Yue Chen Yang Xu Wenxuan Chen Yanan Shao Youfeng Yu Lixia Zhu Lingling Chen Lifang Ruan Precision Probiotics in Agroecosystems: Multiple Strategies of Native Soil Microbiotas for Conquering the Competitor Ralstonia solanacearum mSystems soil microbiome Ralstonia solanacearum precision probiotics multifaceted biocontrol |
| title | Precision Probiotics in Agroecosystems: Multiple Strategies of Native Soil Microbiotas for Conquering the Competitor Ralstonia solanacearum |
| title_full | Precision Probiotics in Agroecosystems: Multiple Strategies of Native Soil Microbiotas for Conquering the Competitor Ralstonia solanacearum |
| title_fullStr | Precision Probiotics in Agroecosystems: Multiple Strategies of Native Soil Microbiotas for Conquering the Competitor Ralstonia solanacearum |
| title_full_unstemmed | Precision Probiotics in Agroecosystems: Multiple Strategies of Native Soil Microbiotas for Conquering the Competitor Ralstonia solanacearum |
| title_short | Precision Probiotics in Agroecosystems: Multiple Strategies of Native Soil Microbiotas for Conquering the Competitor Ralstonia solanacearum |
| title_sort | precision probiotics in agroecosystems multiple strategies of native soil microbiotas for conquering the competitor ralstonia solanacearum |
| topic | soil microbiome Ralstonia solanacearum precision probiotics multifaceted biocontrol |
| url | https://journals.asm.org/doi/10.1128/msystems.01159-21 |
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