Sun Tianyu, Liu Hongwei, Wang Ningqi, Huang Mingcong, Banerjee Samiran, Jousset Alexandre, Xu Yangchun, Shen Qirong, Wang Shimei, Wang Xiaofang, Wei Zhong
Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Key Lab of Organic-Based Fertilizers of China, Jiangsu Collaborative Innovation Center for Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving fertilizers, Nanjing Agricultural University, Nanjing, 210095, China.
College of Agro-Grassland Science, Nanjing Agricultural University, Nanjing, Jiangsu, 210095, People's Republic of China.
Microbiome. 2025 May 19;13(1):126. doi: 10.1186/s40168-025-02120-y.
Streptomyces spp. are known for producing bioactive compounds that suppress phytopathogens. However, previous studies have largely focused on their direct interactions with pathogens and plants, often neglecting their interactions with the broader soil microbiome. In this study, we hypothesized that these interactions are critical for effective pathogen control. We investigated a diverse collection of Streptomyces strains to select those with strong protective capabilities against tomato wilt disease caused by Ralstonia solanacearum. Leveraging a synthetic community (SynCom) established in our lab, alongside multiple in planta and in vitro co-cultivation experiments, as well as transcriptomic and metabolomic analyses, we explored the synergistic inhibitory mechanisms underlying bacterial wilt resistance facilitated by both Streptomyces and the soil microbiome.
Our findings indicate that direct antagonism by Streptomyces is not sufficient for their biocontrol efficacy. Instead, the efficacy was associated with shifts in the rhizosphere microbiome, particularly the promotion of two native keystone taxa, CSC98 (Stenotrophomonas maltophilia) and CSC13 (Paenibacillus cellulositrophicus). In vitro co-cultivation experiments revealed that CSC98 and CSC13 did not directly inhibit the pathogen. Instead, the metabolite of CSC13 significantly enhanced the inhibition efficiency of Streptomyces R02, a highly effective biocontrol strain in natural soil. Transcriptomic and metabolomic analyses revealed that CSC13's metabolites induced the production of Erythromycin E in Streptomyces R02, a key compound that directly suppressed R. solanacearum, as demonstrated by our antagonism tests.
Collectively, our study reveals how beneficial microbes engage with the native soil microbiome to combat pathogens, suggesting the potential of leveraging microbial interactions to enhance biocontrol efficiency. These findings highlight the significance of intricate microbial interactions within the microbiome in regulating plant diseases and provide a theoretical foundation for devising efficacious biocontrol strategies in sustainable agriculture. Video Abstract.
链霉菌属以产生抑制植物病原体的生物活性化合物而闻名。然而，以往的研究主要集中在它们与病原体和植物的直接相互作用上，常常忽略了它们与更广泛的土壤微生物群落的相互作用。在本研究中，我们假设这些相互作用对有效控制病原体至关重要。我们研究了多种链霉菌菌株，以筛选出对由青枯雷尔氏菌引起的番茄青枯病具有强大保护能力的菌株。利用我们实验室建立的合成群落（SynCom），结合多个植物体内和体外共培养实验，以及转录组学和代谢组学分析，我们探索了链霉菌和土壤微生物群落促进青枯病抗性的协同抑制机制。
我们的研究结果表明，链霉菌的直接拮抗作用不足以实现其生物防治效果。相反，防治效果与根际微生物群落的变化有关，特别是促进了两个本地关键分类群，CSC98（嗜麦芽窄食单胞菌）和CSC13（纤维素营养类芽孢杆菌）的生长。体外共培养实验表明，CSC98和CSC13不会直接抑制病原体。相反，CSC13的代谢产物显著提高了链霉菌R02在天然土壤中的抑制效率，R02是一种高效的生物防治菌株。转录组学和代谢组学分析表明，CSC13的代谢产物诱导链霉菌R02产生红霉素E，拮抗试验表明，红霉素E是直接抑制青枯雷尔氏菌的关键化合物。
总的来说，我们的研究揭示了有益微生物如何与本地土壤微生物群落相互作用以对抗病原体，表明利用微生物相互作用提高生物防治效率的潜力。这些发现突出了微生物群落中复杂的微生物相互作用在调节植物病害方面的重要性，并为在可持续农业中设计有效的生物防治策略提供了理论基础。视频摘要。
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