Changes in the soil and rhizosphere microbiomes associated with bacterial wilt decline in the tomato monoculture field

Abstract Background Monoculture farming increases the efficiency of planting and harvesting, but at the same time, exacerbates the severity of soilborne diseases. Disease-suppressive soils are an effective and sustainable resource for managing soilborne diseases in monoculture systems. However, the abiotic and biotic factors contributing to the emergence and function of specific suppressiveness remain elusive, limiting the broader acceptance of suppressive soil in agriculture. Here, we investigated changes in the belowground tomato microbiome during long-term monoculture leading to an outbreak and subsequent suppression of bacterial wilt. We also conducted greenhouse experiments to examine the differences in rhizosphere community and plant performance between disease-suppressive soil and disease-conductive soil. Moreover, we used metagenomics to assess the functional profiles of rhizosphere communities in response to suppressive soil. Results In our long-term tomato monoculture system, wilt incidence steadily increased, culminating in the most severe outbreak in the fifth cropping cycle. Surprisingly, in the seventh crop, wilt symptoms spontaneously declined, signifying a transition toward the disease-suppressive state. Greenhouse disease assays confirmed that the suppressive soil had significantly lower wilt incidence, compared to its disease-conductive counterpart. Drenching tomato seedlings planted in infested soil with rhizosphere soil suspensions from disease-suppressive plots significantly improved the plant growth and physiological characteristics compared to seedlings treated with a conducive soil suspension. The monocropping and disease reduction were associated with shifts in the diversity and abundance of multiple bacteria associated with plant roots, including an enrichment of Bacillus, Pseudomonas, and Streptomyces. Isolates of Pseudomonas and Bacillus from plants growing in suppressive soil antagonized R. solanacearum and significantly decreased the incidence of bacterial wilt in greenhouse trials. Another important change that accompanied the transition towards the disease-suppressive state involved the enrichment of Streptomyces and trace elements (Mn, Ni) in bulk soil. Functional analysis of the suppressive soil metagenome revealed enrichment of genes for the synthesis of antibiotics, polysaccharides, nitrogen metabolism, mineral absorption, and energy production. Conclusions This study is among the first to directly demonstrate that long-term tomato monoculture can induce specific soil suppressiveness against Ralstonia wilt, while also revealing the key changes in soil and rhizosphere microbiomes and their function associated with this phenomenon.