Addition of Earthworms to Continuous Cropping Soil Inhibits the Fusarium Wilt in Watermelon: Evidence Under Both Field and Pot Conditions

Fusarium wilt is a devastating soilborne disease that significantly reduces watermelon production worldwide. This disease is caused by Fusarium oxysporum subsp. niveum (E.F.Sm.) W.C. Snyder & H.N.Hansen. Earthworms can influence fungal populations either by consuming or dispersing fungal propagules, making them a promising candidate for the biological control of Fusarium wilt. However, the underlying mechanisms remain poorly understood. In this study, we investigated the effects of adding the local earthworm species Metaphire guillelmi (Michaelsen, 1895) on Fusarium wilt in watermelon under field conditions, laboratory pot experiments, and laboratory pot experiments with sterilized soil. The results demonstrated that, compared to the control, the earthworm addition reduced the population of F. oxysporum by approximately 105 copies/mg and suppressed the incidence of Fusarium wilt by 84.4%. A correlation analysis revealed that the abundance of F. oxysporum was negatively correlated with soil organic matter (SOM), available nitrogen (AN), and available phosphorus (AP). The relative interaction index values indicated that earthworms could enhance SOM and AN levels in the soil. A two-factor network relationship analysis showed that the earthworm addition could inhibit bacteria and fungi to stimulate growth of F. oxysporum while restraining them. A metabolomics analysis revealed that most differential metabolites associated with F. oxysporum were upregulated in the presence of earthworms. Overall, M. guillelmi can reduce the occurrence of Fusarium wilt by improving soil fertility, the relationship of F. oxysporum and microorganisms, and may influence the metabolic process, which need further exploration. It is a potential pathway for the biocontrol of Fusarium wilt.