Bio-organic soil amendment promotes the suppression of Ralstonia solanacearum by inducing changes in the functionality and composition of rhizosphere bacterial communities

Stimulating the development of soil suppressiveness against certain pathogens represents a sustainable solution toward reducing pesticide use in agriculture. However, understanding the dynamics of suppressiveness and the mechanisms leading to pathogen control remain largely elusive. Here, we investigated the mechanisms used by the rhizosphere microbiome induces bacterial wilt disease suppression in a long-term field experiment where continuous application of bio-organic fertilizers (BFs) triggered disease suppressiveness when compared to chemical fertilizer application. We further demonstrated in a glasshouse experiment that the suppressiveness of the rhizosphere bacterial communities was triggered mainly by changes in community composition rather than only by the abundance of the introduced biocontrol strain. Metagenomics approaches revealed that members of the families Sphingomonadaceae and Xanthomonadaceae with the ability to produce secondary metabolites were enriched in the BF plant rhizosphere but only upon pathogen invasion. We experimentally validated this observation by inoculating bacterial isolates belonging to the families Sphingomonadaceae and Xanthomonadaceae into conducive soil, which led to a significant reduction in pathogen abundance and increase in nonribosomal peptide synthetase gene abundance. We conclude that priming of the soil microbiome with BF amendment fostered reactive bacterial communities in the rhizosphere of tomato plants in response to biotic disturbance.

Automated summary

Stimulating the development of soil suppressiveness against certain pathogens through the manipulation of the rhizosphere microbiome has been shown to be an effective way to reduce pesticide use in agriculture. In this study, we investigated the mechanisms behind the suppression of bacterial wilt disease in tomato plants by the rhizosphere microbiome. We found that changes in community composition, rather than the abundance of biocontrol strains, were responsible for the disease suppressiveness observed in long-term field experiments with bio-organic fertilizers. Metagenomics analysis revealed that certain families of bacteria, such as Sphingomonadaceae and Xanthomonadaceae, were enriched in the rhizosphere when pathogen invasion occurred. Further experiments confirmed that these bacteria were able to significantly reduce pathogen abundance and increase the abundance of genes associated with nonribosomal peptide synthesis. Our findings suggest that priming the soil microbiome with bio-organic fertilizers can promote the development of reactive bacterial communities in the rhizosphere, which contribute to disease suppression.