The fate of Candida tropicalis in the black soldier fly larvae and its nutritional effect suggest indirect interactions

Abstract

Bacteria are known to colonize the insect gut and determine a positive effect on their host's fitness, for example, by providing essential nutrients or improving digestion efficiency. However, information on the colonization of the insect gut by fungi and their nutritional contribution is still scarce and fragmentary. In this study, the presence of Candida tropicalis, a fungus abundant in the black soldier fly (Hermetia illucens, BSF) larvae's gut and environment, was determined in the different gut regions. In addition, metabolites present in larvae fed with a fungus-containing diet were determined by untargeted metabolomics and compared to the C. tropicalis metabolic composition and metabolic changes in the feeding substrate supplemented with the microorganism. Our results indicate that C. tropicalis ceased to be present in the BSF gut after its supplementation in the feeding substrate was stopped, indicating that C. tropicalis does not colonize the gut. Larvae that were reared on diet supplemented with C. tropicalis displayed an increase in the fatty acid biosynthesis pathway, due to an increase in the palmitic and myristic acids that are abundant in C. tropicalis. The presence of C. tropicalis in the substrate caused an increase in threonine, leucine, and isoleucine biosynthesis pathways in the larvae and suggests indirect feeding from the fungal excretions in the substrate. In addition, the lysozyme activity in the larval gut was reduced by the presence of C. tropicalis, suggesting the fungal involvement in the digestive process for increasing fungal survival. This study suggests indirect symbiotic interactions, in which C. tropicalis thrives in the BSF larvae's environment and manipulates BSF digestive enzyme production to survive in this environment, but on the other hand, BSF larvae benefit metabolically from the C. tropicalis presence in its surrounding environment.