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

Abstract

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 genebased 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 ω-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 LC 50 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.

Predation potential of the earwig Euborellia annulipes on fruit fly larvae and trophic interactions with the parasitoid Diachasmimorpha longicaudata

“…Previous studies demonstrated that parasitoids do not reject a D. longicaudata-parasitized host before examining it internally with the ovipositor, suggesting that internal conditions or marker pheromones deposited inside the host are responsible for not parasitizing it (Cancino et al, 2012;Devescovi et al, 2020;Montoya et al, 2003). Contrary to the pattern reported in the literature that oviposition by larval parasitoids changes only internal host conditions (Nufio & Papaj, 2001), there is growing evidence that larval parasitism can also induce chemical changes in the host epicuticle (Kryukov et al, 2022;Lebreton et al, 2010). In addition, generalist predators seem to be capable of recognizing parasitized prey on the basis of external cues (Labbe et al, 2006;Moral, Demetrio, et al, 2017;Naranjo, 2007).…”

The endosymbiotic bacterium Wolbachia (Rickettsiales) alters larval metabolism of the parasitoid Habrobracon hebetor (Hymenoptera: Braconidae)

“…is the dominant bacterium in the wax moth larvae cuticle, while various Enterobacteria and Pseudomonas spp. may also be dominant or subdominant in host integument (Allonsius et al, 2019; Kryukov et al, 2022). A similar dependence of the parasitoid microbiota on the host's microbiome was observed in the endoparasitic wasp Nasonia vitripennis (Duan et al, 2020).…”

Effects of passages through an insect or a plant on virulence and physiological properties of the fungus Metarhizium robertsii

“…On the contrary, in the present article, the plant- and insect-passaged reisolates demonstrated significantly lowered virulence to two insect species: (a) the wax moth that was used for the passaging and (b) the Colorado potato beetle, which represents a target host from another insect order. Notably, larvae of these two insects possess strikingly dissimilar epicuticular lipid composition ( Tomilova et al, 2019 ; Kryukov et al, 2022 ). In a series of independent studies, it has been reported that passaging through insects may not alter fungal virulence ( Hall, 1980 ; Ignoffo et al, 1982 ; Brownbridge, Costa & Jaronski, 2001 ; Vandenberg & Cantone, 2004 ; Eckard et al, 2014 ; Holderman et al, 2017 ; White et al, 2021 ), and only a few articles indicate its weakening ( Hussain et al, 2010 ).…”