Root-Associated Antagonistic Pseudomonas spp. Contribute to Soil Suppressiveness against Banana Fusarium Wilt Disease of Banana

Members of the microbiotas colonizing the plant endophytic compartments and the surrounding bulk and rhizosphere soil play an important role in determining plant health. However, the relative contributions of the soil and endophytic microbiomes and their mechanistic roles in achieving disease suppression remain elusive. To disentangle the relative importance of the different microbiomes in the various plant compartments in inhibiting pathogen infection, we conducted a field experiment to track changes in the composition of microbial communities in bulk and rhizosphere soil and of root endophytes and leaf endosphere collected from bananas planted on Fusarium-infested orchards in disease-suppressive and disease-conducive soils. We found that the rhizosphere and roots were the two dominant plant parts whose bacterial communities contributed to pathogen suppression. We further observed that Pseudomonas was potentially a key organism acting as a pathogen antagonist, as illustrated by microbial community composition and network analysis. Subsequently, culturable pathogen-antagonistic Pseudomonas strains were isolated, and their potential suppressive functions or possible antibiosis in terms of auxin or siderophore synthesis and phosphate solubilization were screened to analyze the mode of action of candidate disease-suppressive Pseudomonas strains. In a follow-up in vivo and greenhouse experiment, we revealed that microbial consortia of culturable Pseudomonas strains P8 and S25 (or S36), isolated from banana plantlet rhizosphere and roots, respectively, significantly suppressed the survival of pathogens in the soil, manipulated the soil microbiome, and stimulated indigenous beneficial microbes. Overall, our study demonstrated that root-associated microbiomes, especially the antagonistic Pseudomonas sp. components, contribute markedly to soil suppression of banana Fusarium wilt. IMPORTANCE Soil suppression of Fusarium wilt disease has been proven to be linked with the local microbial community. However, the contribution of endophytic microbes to disease suppression in wilt-suppressive soils remains unclear. Moreover, the key microbes involving in Fusarium wilt-suppressive soils and in the endophytic populations have not been fully characterized. In this study, we demonstrate that root-associated microbes play vitally important roles in disease suppression. Root-associated Pseudomonas consortia were recognized as a key component in inhibiting pathogen abundance associated with the host banana plants. This finding is crucial to developing alternate strategies for soilborne disease management by harnessing the plant microbiome.