Shared Core Microbiome and Functionality of Key Taxa Suppressive to Banana Fusarium Wilt

Abstract

Microbial contributions to natural soil suppressiveness have been reported for a range of plant pathogens and cropping systems. To disentangle the mechanisms underlying suppression of banana Panama disease caused by Fusarium oxysporum f. sp. cubense tropical race 4 (Foc4), we used amplicon sequencing to analyze the composition of the soil microbiome from six separate locations, each comprised of paired orchards, one potentially suppressive and one conducive to the disease. Functional potentials of the microbiomes from one site were further examined by shotgun metagenomic sequencing after soil suppressiveness was confirmed by greenhouse experiments. Potential key antagonists involved in disease suppression were also isolated, and their activities were validated by a combination of microcosm and pot experiments. We found that potentially suppressive soils shared a common core community with relatively low levels of F. oxysporum and relatively high proportions of Myxococcales, Pseudomonadales, and Xanthomonadales, with five genera, Anaeromyxobacter, Kofleria, Plesiocystis, Pseudomonas, and Rhodanobacter being significantly enriched. Further, Pseudomonas was identified as a potential key taxon linked to pathogen suppression. Metagenomic analysis showed that, compared to the conducive soil, the microbiome in the disease suppressive soil displayed a significantly greater incidence of genes related to quorum sensing, biofilm formation, and synthesis of antimicrobial compounds potentially active against Foc4. We also recovered a higher frequency of antagonistic Pseudomonas isolates from disease suppressive experimental field sites, and their protective effects against banana Fusarium wilt disease were demonstrated under greenhouse conditions. Despite differences in location and soil conditions, separately located suppressive soils shared common characteristics, including enrichment of Myxococcales, Pseudomonadales, and Xanthomonadales, and enrichment of specific Pseudomonas populations with antagonistic activity against the pathogen. Moreover, changes in functional capacity toward an increase in quorum sensing, biofilm formation, and antimicrobial compound synthesizing involve in disease suppression.