Parasitoid venom alters the lipid composition and development of microorganisms on the wax moth cuticle

Ectoparasitoids may change host metabolism, making the environment more favorable for the development of their larvae. These alterations may also be suitable for growth and proliferation of commensal microorganisms and pathogens. This is especially important in relation to cuticular microbiota, with which ectoparasitoids interact directly. However, biochemical and microbiological changes occurring on insect cuticles in response to parasitoid venoms are insufficiently understood. We assayed the biochemical and microbiological changes in cuticles of larvae of the wax moth, Galleria mellonella (L.) (Lepidoptera: Pyralidae), after envenomation by Habrobracon brevicornis (Wesmael) (Hymenoptera: Braconidae). In particular, lipid composition in the epicuticle, total nitrogen (N) and carbon (C) amounts in the cuticle, bacterial colony-forming unit (CFU) counts, and bacterial community structure (16S rRNA gene-based metagenomics) on the insect surface were analyzed. The susceptibility of wax moth larvae to the entomopathogenic fungus (EPF) Metarhizium robertsii J.F. Bisch., S.A. Rehner & Humber (Hypocreales: Clavicipitaceae) was also assessed. Envenomation led to an increase in the hydrocarbon amount, as well as alterations in the fatty acid composition of the epicuticle; in particular, a large decrease in the amount of omega-1 hydroxy fatty acids. The total N and C amounts in the cuticle also slightly increased after envenomation. These changes were correlated with a decrease in bacterial diversity and an increase in Enterococcus abundance on the surface of envenomated larvae. Envenomation also led to a substantial increase in larval susceptibility to M. robertsii infection; differences between the LC50 values of envenomated and control larvae were 505 000-fold. We suggest that the hyper-lipidation of the cuticle is related to processes occurring in the host's hemocoel after envenomation by the parasitoid. The effects of the changes in the lipid composition on the proliferation and development of microorganisms are discussed.