Phages enhance both phytopathogen density control and rhizosphere microbiome suppressiveness

Author:

Wang Xiaofang1ORCID,Wang Shuo1,Huang Mingcong1,He Yilin1,Guo Saisai1,Yang Keming12,Wang Ningqi1,Sun Tianyu1,Yang Hongwu3,Yang Tianjie1,Xu Yangchun1,Shen Qirong1,Friman Ville-Petri14ORCID,Wei Zhong1ORCID

Affiliation:

1. 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

2. College of Agro-grassland Science, Nanjing Agricultural University, Nanjing, Jiangsu, China

3. China National Tobacco Corporation Hunan Company, Changsha, Hunan, China

4. Department of Microbiology, University of Helsinki, Helsinki, Finland

Abstract

ABSTRACT 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 Ralstonia solanacearum 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 R. solanacearum 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 Actinobacteria known for antibiotics production and soil suppressiveness. To test if they could have had secondary effects on R. solanacearum biocontrol, we isolated Actinobacteria from Nocardia and Streptomyces genera and tested their suppressiveness to the pathogen in vitro and in planta . We found that these taxa could clearly inhibit R. solanacearum 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. IMPORTANCE Ralstonia solanacearum 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 R. solanacearum , 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.

Funder

MOST | National Natural Science Foundation of China

National Key Research and Development Program of China

MOST |The Postdoctoral Research Funding Program of Jiangsu Province, China

Finnish Research Council

Publisher

American Society for Microbiology

Cited by 1 articles. 订阅此论文施引文献 订阅此论文施引文献,注册后可以免费订阅5篇论文的施引文献,订阅后可以查看论文全部施引文献

1. Meddling with the microbiota: Fungal tricks to infect plant hosts;Current Opinion in Plant Biology;2024-12

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