Parasitoid envenomation alters the Galleria mellonella midgut microbiota and immunity, thereby promoting fungal infection

Abstract

Gut bacteria influence the development of different pathologies caused by bacteria, fungi and parasitoids in insects. Wax moth larvae became more susceptible to fungal infections after envenomation by the ectoparasitoid Habrobracon hebetor . In addition, spontaneous bacterioses occurred more often in envenomated larvae. We analyzed alterations in the midgut microbiota and immunity of the wax moth in response to H. hebetor envenomation and topical fungal infection ( Beauveria bassiana ) alone or in combination using 16S rRNA sequencing, an analysis of cultivable bacteria and a qPCR analysis of immunity- and stress-related genes. Envenomation led to a predominance shift from enterococci to enterobacteria, an increase in CFUs and the upregulation of AMPs in wax moth midguts. Furthermore, mycosis nonsignificantly increased the abundance of enterobacteria and the expression of AMPs in the midgut. Combined treatment led to a significant increase in the abundance of Serratia and a greater upregulation of gloverin. The oral administration of predominant bacteria ( Enterococcus faecalis, Enterobacter sp. and Serratia marcescens ) to wax moth larvae synergistically increased fungal susceptibility. Thus, the activation of midgut immunity might prevent the bacterial decomposition of envenomated larvae, thus permitting the development of fungal infections. Moreover, changes in the midgut bacterial community may promote fungal killing.

Peer Review #3 of "Combined effect of the entomopathogenic fungus Metarhizium robertsii and avermectins on the survival and immune response of Aedes aegypti larvae (v0.1)"

“…This effect may be associated with impaired intestinal peristalsis as well as changes in the level of PO and antibacterial activity in the initial stages of toxicosis and fungal infection. Similar effects have been observed in terrestrial insects following topical infection by fungi (Wei et al, 2017;Ramirez et al, 2018;Polenogova et al, 2019) and are associated with the redistribution of immune responses between the cuticle and the gut. In mosquito larvae, the fungus comes into direct contact with gut microbiota, which may exhibit fungistatic properties (Sivakumar et al, 2017;Zhang et al, 2017, etc.…”

Interplay between Fungal Infection and Bacterial Associates in the Wax Moth Galleria mellonella under Different Temperature Conditions

“…Direct and indirect interactions between fungi and bacteria may lead to both antagonistic and synergistic effects on survival [ 2 , 4 , 5 , 6 ]. In addition, interrelations between fungi and bacteria in insect hosts may be mediated by complex environmental factors, such as temperature, chemicals, or parasitoids, that have an influence on the outcome of the disease [ 7 , 8 ]. However, these immune-ecological studies are just beginning to develop.…”

The microbiome of the invertebrate model host Galleria mellonella is dominated by Enterococcus

“…To the best of our knowledge, only four studies have used high-throughput 16S rRNA gene sequencing for the characterization of the gut microbiota of the larvae. The focus of these studies was, however, on how G. mellonella manages its gut microbiota during metamorphosis, on the influence of antibiotic feeding on alterations in antibiotic resistance gene pool in the gut microbiota, and the effect of particular Photorhabdus strains and envenomation by the ectoparasitoid Habrobracon hebetor on the gut microbiota [4][5][6][7]. The bacterial diversity of different body niches (e.g.…”