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Fungal infections and toxicoses caused by insecticides may alter microbial communities and immune responses in the insect gut. We investigated the effects of Metarhizium robertsii fungus and avermectins on the midgut physiology of Colorado potato beetle larvae. We analyzed changes in the bacterial community, immunity- and stress-related gene expression, reactive oxygen species (ROS) production, and detoxification enzyme activity in response to topical infection with the M. robertsii fungus, oral administration of avermectins, and a combination of the two treatments. Avermectin treatment led to a reduction in microbiota diversity and an enhancement in the abundance of enterobacteria, and these changes were followed by the downregulation of Stat and Hsp90, upregulation of transcription factors for the Toll and IMD pathways and activation of detoxification enzymes. Fungal infection also led to a decrease in microbiota diversity, although the changes in community structure were not significant, except for the enhancement of Serratia. Fungal infection decreased the production of ROS but did not affect the gene expression of the immune pathways. In the combined treatment, fungal infection inhibited the activation of detoxification enzymes and prevented the downregulation of the JAK-STAT pathway caused by avermectins. The results of this study suggest that fungal infection modulates physiological responses to avermectins and that fungal infection may increase avermectin toxicosis by blocking detoxification enzymes in the gut.

Most invertebrate species exhibit immunological responses that can inactivate and eliminate penetrating parasites. Such immune responses in particular involve the formation of potentially toxic reactive oxygen species (ROS). We explored the immune capabilities of the first-generation (F1) offspring of naturally infected freshwater snails, Lymnaea stagnalis, in response to infection by trematode cercariae under laboratory conditions. The rates of ROS formation and peroxidase activity in the hemolymph of the F1 offspring of L. stagnalis parents infected by an asexual stage of trematodes were significantly higher than in F1 offspring of uninfected parents. Compared to offspring from uninfected parents, the growth rate of F1 snails from infected parents was higher, but survival was lower. After infection of F1 snails by trematode cercariae of Echinoparyphium aconiatum under laboratory conditions, the rate of ROS formation and peroxidase activity in the hemolymph of F1 offspring of uninfected parents increased compared to control snails. This pattern persisted throughout the entire 3-week observation period. In contrast, the rate of ROS formation in the hemolymph of F1 snails from infected parents after experimental infection by E. aconiatum cercariae did not differ from controls, and peroxidase activity even decreased. Thus, trematode parthenitae infection of parents could alter the immune response of their offspring.

Entomopathogenic fungi form different strategies of interaction with their insect hosts. The influence of fungal infection on insect physiology has mainly been studied for generalists (Metarhizium, Beauveria), but studies of specialized teleomorphic species, such as Cordyceps militaris, are rare. We conducted a comparative analysis of the immune reactions of the wax moth Galleria mellonella after injection with blastospores of C. militaris (Cm) and Metarhizium robertsii (Mr) in two doses (400 and 4000 per larva). Cm-injected insects died more slowly and were more predisposed to bacterial infections than Mr-injected insects. It was shown that Cm infection led to a predominance of necrotic death of hemocytes, whereas Mr infection led to apoptotic death of cells. Cm-infected insects produced more dopamine and reactive oxygen species compared to Mr-infected insects. Moreover, Cm injection led to weak inhibition of phenoloxidase activity and slight enhancement of detoxification enzymes compared to Mr-injected insects. Blastospores of Cm that were cultivated in artificial medium (in vitro) and proliferated in wax moth hemolymph (in vivo) were characterized by equal intensity of fluorescence after staining with Calcofluor White. In contrast, Mr blastospores that proliferated in the wax moth had decreased fluorescence intensity compared to Mr blastospores grown in medium. The results showed that insects combat Cm infection more actively than Mr infection. We suggest that Cm uses fewer universal tools of killing than Mr, and these tools are available because of specific interactions of Cm with hosts and adaptation to certain host developmental stages.