Promoting soil microbial-mediated suppressiveness against Fusarium wilt disease by fungal taxa-specific enrichment via crop rotation

Manipulation of the soil microbiome can be used as an effective strategy to alleviate the disease pressure imposed by soilborne diseases in agricultural systems. The use of crop rotation is widely known to exert a level of control on soil-borne diseases by altering the soil chemical and biological properties. However, we still lack an understanding of how different crop rotation systems affect the dynamics and functioning of soil microbiomes. Here, we studied a pineapple-banana rotation system as a model to investigate the emergence of microbial-mediated disease-suppression in a soil highly infested with the pathogen Fusarium oxysporum f. sp. cubense tropical race4 (Foc4) causing banana wilt disease. By using both field and pot experiments, we show the pineapple-banana rotation system to result in a significant decrease of the pathogen number and disease incidence in a soil initially highly infested with the pathogen. We found this pathogen-suppression phenomenon to be linked with detectable shifts in the soil resident fungal taxa. Most importantly, taxa affiliated with Talaromyces pinophilus and Clonostachys rossmaniae were found to be enriched in suppressive soils. We further found the first to also be enriched in the rhizosphere of banana after the rotation with pineapple. Later, we tested for the suppressive potential of these fungal taxa via isolation and pot inoculation. Our results revealed that both Talaromyces pinophilus and Clonostachys rossmaniae isolates are able to antagonize Foc4, thus confirming their biocontrol efficacy. Taken together, our study provides evidence on how crop rotation affects the resident soil microbiome towards the development of disease suppressiveness. We highlight the importance of understanding the dynamic changes in soil biology and validating the mechanisms underpinning suppression to promote practical and directed manipulation in agroecological systems.