Characterizing the Key Agents in a Disease-Suppressed Soil Managed by Reductive Soil Disinfestation

Many agricultural soil management strategies have been shown to be effective in preventing soilborne diseases. However, their underlying mechanisms of action remain unknown. In this study, we used reductive soil disinfestation (RSD), also named anaerobic soil disinfestation (ASD) and biological soil disinfestation (BSD), as a representative method for disease management and cucumber damping-off diseased soil as a model system to identify the disease-suppressive agents in artificially managed soil. The results showed that RSD created a soil environment that was different from that of the diseased soil, where the pH level and the carbon content were greater. Heat treatment and pathogen or soil microbiota self- and cross-reinoculations resulted in the expansion of various soil microbial communities harbored by the two soil environments, as well as various disease incidences. Environmental factors were the primary determinant of the reassembled bacterial community, followed by initial microbiota, whereas initial microbiota was the key driver of the reassembled fungal community. The relative abundances of the bacterial order Sphingobacteriales and fungal order Sordariales, as well as their affiliated genera Sphingobacterium, unclassified genus within Sphingobacteriaceae, Zopfiella, and unclassified genera within Lasiosphaeriaceae and Chaetomiaceae, were negatively correlated with disease incidence and positively associated with RSD-conditioned soil environment. Furthermore, we validated that both the microbial disease-suppressive agent and its adapted abiotic environment contributed to disease suppression. Our results elucidate the abiotic and biotic foundations of soilborne disease suppression under artificial management and highlight that the abiotic environment is as important as the microbial agents in disease suppression. IMPORTANCE Most defined systems have identified microbial elements as the primary factors determining disease suppression, but the involvement of the soil abiotic environment is less defined. The significance of this work is that the soil abiotic environment plays a critical role in the establishment of the soil microbial community and key microbial agents that directly contribute to the prevention of soilborne diseases. We highlight the importance of the soil abiotic environment in disease suppression. Furthermore, we provide a framework for the characterization of disease-suppressing agents in artificially managed soil. These results will gradually close the gap in knowledge on soil environment-microbe interactions.