Aspergillus nidulans Synthesize Insect Juvenile Hormones upon Expression of a Heterologous Regulatory Protein and in Response to Grazing by Drosophila melanogaster Larvae

Abstract

Secondary metabolites are known to serve a wide range of specialized functions including communication, developmental control and defense. Genome sequencing of several fungal model species revealed that the majority of predicted secondary metabolite related genes are silent in laboratory strains, indicating that fungal secondary metabolites remain an underexplored resource of bioactive molecules. In this study, we combine heterologous expression of regulatory proteins in Aspergillus nidulans with systematic variation of growth conditions and observe induced synthesis of insect juvenile hormone-III and methyl farnesoate. Both compounds are sesquiterpenes belonging to the juvenile hormone class. Juvenile hormones regulate developmental and metabolic processes in insects and crustaceans, but have not previously been reported as fungal metabolites. We found that feeding by Drosophila melanogaster larvae induced synthesis of juvenile hormone in A. nidulans indicating a possible role of juvenile hormone biosynthesis in affecting fungal-insect antagonisms.

Heterologous Reconstitution of the Intact Geodin Gene Cluster in Aspergillus nidulans through a Simple and Versatile PCR Based Approach

“…The ged + (NID677) and ged + mdpA-L Δ (NID695) strains were obtained by transformation of the relevant gene targeting substrates into NID74 [39] or NID356, respectively. The gene targeting substrates containing Fragment 1 and Fragment 2 were liberated from pU1111 (NotI) and pU2052 (SwaI), respectively, and gel purified (GFX TM , GE Healthcare) prior to transformation.…”

“…All sequences in the alignments can be retrieved from Genbank, by the following references for the putative halogenases: Aspergillus oryzae ref|XP_001818590.1|, Aspergillus terreus ref|XP_001217599.1| and the A. terreus genome sequence resource at the Broad Institute, Bipolaris sorokiniana gb|EMD66881.1|, Chaetomium chiversii (RadH) gb|ACM42402.1|, Chaetomium globosum ref|XP_001227515.1|, Pochonia chlamydosporia (Rdc2) gb|ADM86580.1| [39] and Talaromyces stipitatus ref|XP_002486044.1|. Intron prediction of the A. terreus ATEG_08460.1 locus was done based on the Augustus gene prediction resource [29].…”

Fungal Secondary Metabolism in the Light of Animal–Fungus Interactions: From Mechanism to Ecological Function

“…In confrontation assays with D. melanogaster larvae, the JH overproduction strain had, however, relative to the reference strain, no dramatic influence on insect development. Interestingly, sesquiterpene formation was enhanced when A. nidulans was exposed to D. melanogaster larval grazing [111]. This insect-induced response possibly compensated for the constitutively enhanced formation of JHs in the smrA-expressing strain and might thus explain why constitutive overproduction of JHs had an only minor influence on the fungivores.…”

“…This combined and flexible investment in secondary metabolites and sexual reproduction probably is a strategy for fungal survival and persistence in predator-rich niches. In addition to sterigmatocystin, further compounds-i.e., emericellamides and some me- [111]. These compounds have hormonal function in various arthropods roterpenoids-were produced in excess when A. nidulans was exposed to springtail grazing.…”

Biocatalytic portfolio of Basidiomycota

“…Underground hyphae and fruiting bodies are vulnerable to a number of threats, including antagonistic and competing fungi and bacteria as well as grazing by invertebrates such as small arthropods, insects, nematodes, mollusks and larger animals [22]. In response, fungi have developed diverse defense mechanisms such as the production of secondary metabolites as defense and/or microbial and fauna control agents [23–25]. Hyphae invading wood or decomposing litter also encounter a range of potentially toxic lignin degradation products and plant defense compounds, including mono- and polyphenolic compounds and resins with high contents of terpenes.…”