Microbial and biochemical basis of a Fusarium wilt-suppressive soil

Authors: CHA, JAE-YUL - Gyeongsang National University; HAN, SANGJO - Korean Bioinformation Center (KOBIC); HONG, HEE-JEON - University Of Cambridge; CHO, HYUNJI - Gyeongsang National University; KIM, DARAN - Gyeongsang National University; KWON, YOUNGHO - Gyeongsang National University; NISLOW, COREY - University Of British Columbia; LEE, YOUNG BOK - Gyeongsang National University; KWON, SONGKYUNG - Yonsei University; KIM, JIHYUN - Yonsei University; CRUSEMANN, MAX - University Of California; MOORE, BRADLEY - University Of California; Thomashow, Linda; Weller, David; KWAK, YOUNG-SIG - Gyeongsang National University

Submitted to: The ISME Journal: Multidisciplinary Journal of Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/3/2015
Publication Date: 6/9/2015
Citation: Cha, J., Han, S., Hong, H., Cho, H., Kim, D., Kwon, Y., Nislow, C., Lee, Y., Kwon, S., Kim, J.F., Crusemann, M., Moore, B.S., Thomashow, L.S., Weller, D.M., Kwak, Y. 2015. Microbial and biochemical basis of a Fusarium wilt-suppressive soil. The ISME Journal: Multidisciplinary Journal of Microbial Ecology. 10:119-129.

Interpretive Summary: Disease-suppressive soils are those soils in which a soil-borne disease does not develop or develops and then later declines in severity even though the pathogen is present, the crop is susceptible and environmental conditions are suitable for disease development. Suppressive soils result from the activity of select groups of beneficial microorganisms that are antagonistic to the target pathogens. In this study, we identified a unique field in Korea that was cropped continuously to strawberry for 15 years and was highly suppressive to Fusarium wilt, a devastating soil-borne disease that attacks many important crops. We demonstrated that Fusarium wilt was naturally controlled in this monoculture strawberry field by the beneficial bacterium Streptomyces that produces a novel antibiotic. Our results highlight the role of natural antibiotics as weapons in the microbial warfare in the rhizosphere that leads to the protection of roots from pathogens. Suppressive soils occur worldwide and allow framers to naturally control certain soilborne diseases without the application of chemical pesticides.

Technical Abstract: Crops lack genetic resistance to most necrotrophic soil-borne pathogens and parasitic nematodes that are ubiquitous in agroecosystems worldwide. To overcome this disadvantage, plants recruit and nurture specific group of antagonistic microorganisms from the soil microbiome to defend their roots against pathogens and other pests. The best example of this microbe-based defense of roots is observed in disease-suppressive soils in which the suppressiveness is induced by continuously growing crops that are susceptible to a pathogen. Suppressive soils occur globally yet the microbial basis of most is still poorly described. Fusarium wilt, caused by Fusarium oxysporum f. sp. fragariae is a major disease of strawberry and is naturally suppressed in Korean fields that have undergone continuous strawberry monoculture. Here we show that members of the genus Streptomyces are the specific bacterial components of the microbiome responsible for the suppressiveness that controls Fusarium wilt of strawberry. Furthermore, genome sequencing revealed that Streptomyces griseus, which produces a novel thiopetide antibiotic, is a key species involved in the suppressiveness. Finally, chemical-genetic studies demonstrated that S. griseus antagonizes F. oxysporum by interfering with fungal cell wall synthesis. An attack by F. oxysporum initiates a defensive “cry for help” by strawberry root and the mustering of microbial defenses led by Streptomyces. These results provide a model for future studies to elucidate the basis of microbially-based defense systems and soil suppressiveness from the field to the molecular level.