Shanshan Liu, Shuxian Wang, Jingyuan Zhang, Chengyuan Tao, Mohammadhossein Ravanbakhsh, Xu Xu, Kaiqi Wen, Dandan Xiang, Ou Sheng, Zongzhuan Shen, Chunyu Li, Rong Li, Qirong Shen, George A Kowalchuk
{"title":"Host-guided microbiome-metabolite interactions enable cross-kingdom SynComs for disease suppression.","authors":"Shanshan Liu, Shuxian Wang, Jingyuan Zhang, Chengyuan Tao, Mohammadhossein Ravanbakhsh, Xu Xu, Kaiqi Wen, Dandan Xiang, Ou Sheng, Zongzhuan Shen, Chunyu Li, Rong Li, Qirong Shen, George A Kowalchuk","doi":"10.1186/s40168-026-02430-9","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>The plant microbiome plays a crucial role in enhancing disease resistance, yet microbiome-based plant protection strategies remain limited by an incomplete understanding of how host selection, microbial interactions, and rhizosphere chemistry jointly shape pathogen suppression.</p><p><strong>Results: </strong>Here, we adopt a \"learning from nature\" approach to design synthetic microbial communities (SynComs) that recapitulate naturally evolved disease-suppressive interactions, using banana Fusarium wilt as a model system. High-throughput profiling revealed that both bacterial and fungal communities contribute to varietal resistance. Resistance-associated microbial taxa were identified and isolated to assemble bacterial, fungal, and cross-kingdom SynComs representative of resistant versus susceptible hosts. SynComs derived from resistant varieties suppressed pathogen growth more effectively than those from susceptible hosts, with cross-kingdom SynComs exhibiting the strongest effects. Cross-kingdom SynCom inoculation significantly reduced disease severity and restructured both the composition and functional potential of the rhizosphere microbiome. Integrative transcriptomic and metabolomic analyses revealed coordinated host metabolic reprogramming, characterized by increased accumulation of diverse metabolites, including alkaloids, amino acids, and flavonoids. Notably, supplementation with resistance-associated rhizosphere metabolites, such as stearic acid and shikimic acid, further enhanced disease suppression.</p><p><strong>Conclusions: </strong>Together, our findings establish a mechanistic framework in which host-guided microbiome assembly and metabolite-mediated interactions jointly enable effective cross-kingdom SynComs for disease suppression, providing ecological principles for microbiome-based plant protection strategies. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":" ","pages":""},"PeriodicalIF":14.9000,"publicationDate":"2026-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC13455229/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiome","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40168-026-02430-9","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: The plant microbiome plays a crucial role in enhancing disease resistance, yet microbiome-based plant protection strategies remain limited by an incomplete understanding of how host selection, microbial interactions, and rhizosphere chemistry jointly shape pathogen suppression.
Results: Here, we adopt a "learning from nature" approach to design synthetic microbial communities (SynComs) that recapitulate naturally evolved disease-suppressive interactions, using banana Fusarium wilt as a model system. High-throughput profiling revealed that both bacterial and fungal communities contribute to varietal resistance. Resistance-associated microbial taxa were identified and isolated to assemble bacterial, fungal, and cross-kingdom SynComs representative of resistant versus susceptible hosts. SynComs derived from resistant varieties suppressed pathogen growth more effectively than those from susceptible hosts, with cross-kingdom SynComs exhibiting the strongest effects. Cross-kingdom SynCom inoculation significantly reduced disease severity and restructured both the composition and functional potential of the rhizosphere microbiome. Integrative transcriptomic and metabolomic analyses revealed coordinated host metabolic reprogramming, characterized by increased accumulation of diverse metabolites, including alkaloids, amino acids, and flavonoids. Notably, supplementation with resistance-associated rhizosphere metabolites, such as stearic acid and shikimic acid, further enhanced disease suppression.
Conclusions: Together, our findings establish a mechanistic framework in which host-guided microbiome assembly and metabolite-mediated interactions jointly enable effective cross-kingdom SynComs for disease suppression, providing ecological principles for microbiome-based plant protection strategies. Video Abstract.
期刊介绍:
Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.