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, China.
College of Agro-grassland Science, Nanjing Agricultural University, Nanjing, Jiangsu, China.
mBio. 2024 Jun 12;15(6):e0301623. doi: 10.1128/mbio.03016-23. Epub 2024 May 23.
Bacteriophages, viruses that specifically target plant pathogenic bacteria, have emerged as a promising alternative to traditional agrochemicals. However, it remains unclear how phages should be applied to achieve efficient pathogen biocontrol and to what extent their efficacy is shaped by indirect interactions with the resident microbiota. Here, we tested if the phage biocontrol efficacy of phytopathogenic bacterium can be improved by increasing the phage cocktail application frequency and if the phage efficacy is affected by pathogen-suppressing bacteria already present in the rhizosphere. We find that increasing phage application frequency improves density control, leading to a clear reduction in bacterial wilt disease in both greenhouse and field experiments with tomato. The high phage application frequency also increased the diversity of resident rhizosphere microbiota and enriched several bacterial taxa that were associated with the reduction in pathogen densities. Interestingly, these taxa often belonged to known for antibiotics production and soil suppressiveness. To test if they could have had secondary effects on biocontrol, we isolated Actinobacteria from and genera and tested their suppressiveness to the pathogen and . We found that these taxa could clearly inhibit growth and constrain bacterial wilt disease, especially when combined with the phage cocktail. Together, our findings unravel an undiscovered benefit of phage therapy, where phages trigger a second line of defense by the pathogen-suppressing bacteria that already exist in resident microbial communities.
is a highly destructive plant-pathogenic bacterium with the ability to cause bacterial wilt in several crucial crop plants. Given the limitations of conventional chemical control methods, the use of bacterial viruses (phages) has been explored as an alternative biological control strategy. In this study, we show that increasing the phage application frequency can improve the density control of , leading to a significant reduction in bacterial wilt disease. Furthermore, we found that repeated phage application increased the diversity of rhizosphere microbiota and specifically enriched Actinobacterial taxa that showed synergistic pathogen suppression when combined with phages due to resource and interference competition. Together, our study unravels an undiscovered benefit of phages, where phages trigger a second line of defense by the pathogen-suppressing bacteria present in resident microbial communities. Phage therapies could, hence, potentially be tailored according to host microbiota composition to unlock the pre-existing benefits provided by resident microbiota.
噬菌体是一种专门针对植物病原菌的病毒，已成为传统农用化学品的一种有前途的替代品。然而，目前尚不清楚噬菌体应该如何应用才能实现有效的病原体生物防治，以及它们的功效在多大程度上受到与驻留微生物群落的间接相互作用的影响。在这里，我们测试了通过增加噬菌体鸡尾酒应用频率是否可以提高植物病原菌的噬菌体生物防治效果，以及噬菌体的功效是否受到根际中已经存在的抑制病原体的细菌的影响。我们发现，增加噬菌体的应用频率可以改善密度控制，从而在温室和田间试验中明显减少番茄的细菌性萎蔫病。高噬菌体应用频率还增加了驻留根际微生物群落的多样性，并丰富了与病原体密度降低相关的几个细菌分类群。有趣的是，这些分类群通常属于已知的抗生素产生和土壤抑制性。为了测试它们是否对生物防治有二次影响，我们从 和 属中分离出放线菌，并测试它们对病原体 和 的抑制作用。我们发现，这些分类群可以明显抑制 的生长并限制细菌性萎蔫病，特别是当与噬菌体鸡尾酒结合使用时。总之，我们的研究结果揭示了噬菌体治疗的一个未被发现的好处，即噬菌体通过已经存在于驻留微生物群落中的病原菌抑制细菌触发第二道防线。
