Transcriptional responses of Folsomia candida upon exposure to Aspergillus nidulans secondary metabolites in single and mixed diets

Genetic and molecular evidence to support the hypothesis that fungal secondary metabolites play a significant role in protecting the fungi against fungivory is scarce. We investigated the impact of fungal secondary metabolites on transcript regulation in the fungivorous springtail Folsomia candida feeding on mixed vs. single diets. Aspergillus nidulans, which is able to produce secondary metabolites including sterigmatocystin, and a knockout mutant with reduced secondary metabolism (A. nidulans ΔLaeA) were combined with the high quality fungus Cladosporium cladosporioides as mixed diets or offered as single diets. We hypothesized that (i) A. nidulans WT triggers more genes associated with stress responses compared to the A. nidulans ΔLaeA strain with suppressed secondary metabolism, (ii) C. cladosporioides causes significantly different transcript regulation than the A. nidulans strains ΔLaeA and WT, and (iii) mixed diets will cause significantly different transcript expression levels than single diets. All three hypotheses are generally supported regardless of the fact that functions of many of the differentially transcribed genes are still enigmatic and that a relatively subtle response, devoid of characteristic stress response genes, was observed towards the toxic fungi in the diet. The wild type A. nidulans strain elicited 30% more differentially expressed genes than the ΔLaeA mutant strain. Differentially expressed genes were not observed in the mixture diet of the C. cladosporoides × A. nidulans WT diet, indicating selective grazing on C. cladosporoides. The results bring molecular evidence for the existence of a link between fungal secondary metabolites and responses in springtails supporting the hypothesis that fungal secondary metabolites act as a shield against fungivory.