Constraining Factors and Enhancement Strategies of Phage Therapy in Controlling Soil Biological Pollution

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National Natural Science Foundation of China (Nos. 42090064, 42007025, 42277113), and the Natural Science Foundation of Jiangsu Province of China (BK20200533)

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    Soil serves as a natural habitat for microorganisms, hosting both beneficial and pathogenic species that can either promote plant growth or pose risks to human and animal health. Pathogenic bacteria, such as Ralstonia solanacearum and Erwinia amylovora, which are soil-borne plant pathogens, can infect economically important crops, resulting in significant agricultural losses. Likewise, common human pathogens like Escherichia coli and Salmonella can persist in soil over extended periods, presenting severe health risks through direct or indirect contact. The presence of pathogenic bacteria in soil contributes to soil biological contamination, leading to reduced crop yields, environmental degradation, and safety hazards, which have garnered considerable attention. Controlling the number of these pathogenic bacteria within a safe range is a requirement of One Heath. Numerous studies have demonstrated the crucial role of beneficial microorganisms in the soil in controlling the invasion of pathogenic bacteria. Among them, bacteriophages, which are viruses that selectively infect bacteria, are widely distributed in the environment. Compared to bacteria and fungi, bacteriophages possess advantages such as specific targeting capabilities, rapid lysis, and minimal disruption to the environment, making them an increasingly prominent focus of research. However, similar to other control strategies, enhancing the stability of bacteriophage application in soil remains a significant challenge. Here we discuss the stabilities of bacteriophages in reducing pathogenic bacteria as well as soil biological pollutions by summarizing the following points: 1)the host spectrum and population of bacteriophages in the soil, 2)the polymorphism of pathogenic bacteria, and 3)the potential impacts of soil factors such as temperature, pH, structure, nutrients, and multiple pollutants on the bacteriophage's antibacterial effects in the soil. For bacteriophages, the host spectrum determines the availability of host bacteria in the soil, which affects the bacteriophages' ability to survive in the soil. The more bacteriophages there are around the target pathogenic bacteria, the higher the chance of infecting them, thus, increasing the frequency of bacteriophage-pathogen interactions and the probability of successful infection. As for pathogenic bacteria, they possess a high degree of ecological and genetic diversity in the field and have abundant anti-bacteriophage systems, which limits the effectiveness of individual bacteriophages in suppressing them. Various environmental factors also influence the colonization and functional performance of bacteriophages in the soil. For instance, high temperatures and inappropriate pH can inactivate bacteriophages, soil particles may adsorb bacteriophages and reduce their migration ability, nutrient levels can alter bacteriophage-bacteria interactions, and soil pollutants like heavy metals and antibiotics may affect bacteriophage activity. To enhance the stability of bacteriophage-mediated control of soil-borne pathogens, strategies such as constructing efficient bacteriophage cocktails, improving bacteriophage product formulations, and optimizing bacteriophage application techniques are proposed. This review provides a theoretical basis and technical support for establishing a comprehensive bacteriophage therapy for soil-borne pathogenic bacteria.

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WANG Xiaofang, JIANG Gaofei, WANG Shuo, YANG Keming, XU Yangchun, SHEN Qirong, WEI Zhong. Constraining Factors and Enhancement Strategies of Phage Therapy in Controlling Soil Biological Pollution[J]. Acta Pedologica Sinica,2023,60(5):1378-1388.

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  • Received:July 11,2023
  • Revised:July 31,2023
  • Adopted:September 04,2023
  • Online: September 04,2023
  • Published: September 28,2023