Effects of mycotoxin-producing fungi on the fitness and gut bacterial community of the soil springtail Folsomia candida

Abstract

ABSTRACT Mycotoxin-producing fungi are widespread and their adverse effects on mammals have been investigated; however, their impacts on soil invertebrates are not fully understood. Folsomia candida is a model soil arthropod that represents an important part of the soil invertebrate community. This study investigated the consequences of F. candida grazing on mycotoxin-producing fungi Fusarium verticillioides, F. graminearum, Aspergillus ochraceus, and A. nidulans. Consuming mycotoxin-producing fungi affected the body size and reproductive ability of F. candida, and altered the gut bacterial composition, with decreased Proteobacteria and increased Actinobacteria (Microbacterium) abundances. Notably, the abundance of foodborne fungi can be detected. Furthermore, certain bacteria isolated from F. candida’s gut inhibited the growth of corresponding mycotoxin-producing fungi. The gut bacteria that inhibited mycotoxin-producing fungi growth in Aspergillus groups were also associated with poor fitness parameters and larger disruption in gut microbiota. Importantly, switching back to yeast diets reversed both the fitness parameters and gut bacterial composition. Together, our study demonstrated that grazing of mycotoxin-producing fungi by F. candida resulted in reduced physiological parameters and disturbed the gut bacterial community, and those changes can be restored by switching back to yeast diets, which indicates a strong resilience of springtails to mycotoxin-producing fungi.IMPORTANCEMycotoxin-producing fungi are widespread in nature and raise concerns for human and livestock health. Although they share the same ecosystem, interactions between mycotoxin-producing fungi and soil arthropods are not well understood. In this study, we report an unexpected finding that the soil arthropod Folsomia candida is rather tolerant to these mycotoxin-producing fungi. F. candida can survive solely on mycotoxin-producing fungi as a food source with reduced physiological parameters. Moreover, the gut microbial community is disturbed by mycotoxin-producing fungi, and some of the bacteria isolated from F. candida’s gut can inhibit the growth of corresponding fungi. Notably, the altered physiological parameters and gut microbiota are restored when a normal diet is reintroduced, suggesting F. candida’s resilience to mycotoxin-producing fungi. These findings clarify the impact of toxin-producing diets on F. candida, shedding light on how organisms can build resilience to environmental stimuli.

Keywords

• Folsomia candida
• mycotoxin-producing fungi
• fitness parameter
• gut bacteria
• resilience