Earthworms reduce the accumulation of soil-borne pathogens in strawberry by altering the gut microbiome and physiological characteristics

Pathogenic fungi cause economic loss to many crops including strawberry, highlighting the need for control using sustainable eco-friendly strategies. Earthworm casts effectively reduce the occurrence of soil-borne diseases. However, the interactions between earthworms and soil-borne pathogenic fungi and their underlying mechanisms remain insufficiently understood in strawberry. This study investigated the effects of the pathogenic fungi Fusarium oxysporum and Alternaria alstroemeriae on the structure and composition of the microbial communities in the drilosphere soil and earthworm gut using high-throughput sequencing. The impact of these pathogenic fungi on functional gene expression in earthworms was determined using transcriptomic analysis. Applying F. oxysporum and A. alstroemeriae with earthworms significantly altered the physicochemical properties of the drilosphere soil, reduced the fungal alpha diversity therein, and increased the abundance of potentially beneficial Pseudomonas spp. and Bacillus spp. The presence of the pathogenic fungi increased the alpha diversity and habitat niche breadth of the fungal community in the earthworm gut. However, there was a significant reduction in the relative abundance of potentially pathogenic fungi to plants and animals in the earthworm gut. Earthworms had a positive legacy effect on the abundance of beneficial bacteria in the rhizosphere and enhanced strawberry biomass. Transcriptomic analysis demonstrated that earthworms activated α-linolenic acid and glycerophospholipid metabolism but downregulated the Toll-like receptor pathway, mitigating excessive immune responses. In summary, earthworms suppress soil-borne pathogenic fungi in strawberry via an integrated mechanism involving the restructuring of the gut microbiota, enrichment of biocontrol agents in the drilosphere, and coordination of host immunity, offering a novel paradigm for pest management and sustainable means for strawberry cultivation.