Host-guided microbiome-metabolite interactions enable cross-kingdom SynComs for disease suppression.

IF 14.9 1区 生物学 Q1 MICROBIOLOGY
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
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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.

宿主引导的微生物-代谢物相互作用使跨界syncom能够抑制疾病。
背景:植物微生物组在增强抗病性方面起着至关重要的作用,然而基于微生物组的植物保护策略仍然受到对寄主选择、微生物相互作用和根际化学如何共同形成病原体抑制的不完全理解的限制。结果:在这里,我们采用“向自然学习”的方法来设计合成微生物群落(SynComs),这些群落概括了自然进化的疾病抑制相互作用,以香蕉枯萎病为模型系统。高通量分析显示,细菌和真菌群落对品种抗性都有贡献。鉴定并分离出与耐药相关的微生物分类群,组装耐药与敏感宿主的细菌、真菌和跨界SynComs代表。来自抗性品种的SynComs比来自敏感宿主的SynComs更有效地抑制了病原体的生长,其中跨界的SynComs效果最强。跨界SynCom接种显著降低了疾病严重程度,并重组了根际微生物组的组成和功能潜力。综合转录组学和代谢组学分析揭示了宿主代谢重编程的协调性,其特征是多种代谢物的积累增加,包括生物碱、氨基酸和类黄酮。值得注意的是,补充与抗性相关的根际代谢物,如硬脂酸和莽草酸,进一步增强了疾病抑制。总之,我们的研究结果建立了一个机制框架,在这个框架中,宿主引导的微生物组组装和代谢物介导的相互作用共同实现了有效的跨界SynComs疾病抑制,为基于微生物组的植物保护策略提供了生态学原理。视频摘要。
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来源期刊
Microbiome
Microbiome MICROBIOLOGY-
CiteScore
21.90
自引率
2.60%
发文量
198
审稿时长
4 weeks
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.
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