Deterministic assembly of rhizosphere bacterial community enables predictable and stable suppression of Verticillium wilt via microbial homeostasis.

Abstract

Background: The rhizosphere microbiota plays essential roles in maintaining normal physiological function and preventing disease in plants. However, the mechanisms by which soil-borne pathogens break through the microbial defense line in the rhizosphere to infect the host are not well understood.

Results: In this study, we observed that the relative abundance of Verticillium dahliae does not significantly differ between healthy and diseased rhizospheres, but the root-associated microbial community structure changes substantially. The invasion of pathogens shifts the assembly process of the microbial community from deterministic to stochastic, making it difficult to predict the disease resistance function of the rhizosphere microbial community. An increase in stochasticity promotes the rapid proliferation of opportunistic bacteria, which deplete carbon sources, disrupt the balance of the original microbial community, and reduce network stability. Consequently, the depletion of beneficial microbes leads to rhizosphere dysbiosis, while fungal pathogenic allies gain a competitive advantage, thereby facilitating the progression of Verticillium wilt. These results are further validated by constructing synthetic microbial communities (SynComs) using strains enriched in different ecological processes. Healthy plants maintain their health by recruiting beneficial microorganisms through deterministic processes. Moreover, the disease-suppressive efficacy of SynComs governed by deterministic processes was less affected by inoculation timing or concentration, making their functional outcomes more predictable. In contrast, the disease resistance levels of SynComs governed by stochastic processes are more sensitive to inoculation timing and concentration, making their function more unpredictable.

Conclusions: Overall, our findings emphasize the potential of SynComs designed according to community assembly principles to combat soil-borne diseases, with deterministically assembled SynComs providing more durable disease resistance than stochastically assembled ones. Video Abstract.