A Comparative Analysis of Immune Response, Gut Microbiota, and Susceptibility to Bacillus thuringiensis Bacteria in the Colorado Potato Beetle Leptinotarsa decemlineata

Bacillus thuringiensis-based biological insecticides are highly specific to various types of insects, while being considered environmentally safe. The Colorado potato beetle Leptinotarsa decemlineata is one of the most common insect pests of solanaceous crops worldwide. Its wide distribution across different climatic zones (i.e. high ecological plasticity) and rapid development of the resistance to diverse chemical insecticides raise the question of the mechanisms underlying these two fundamental properties of L. decemlineata. In this study, the indices of cell-mediated and humoral immunity (phenoloxidase and antibacterial systems), activity of antioxidant and detoxification enzymes, gut microbiota, and susceptibility to B. thuringiensis bacteria were studied in the larvae of L. decemlineata from different districts of the Novosibirsk Oblast (NSO). The total hemocyte count and lysozyme-like antibacterial activity in the hemolymph of insects from the Vengerovsky District were 1.5–2 times higher than in the larvae from the Ordynsky District. The activity of detoxification enzymes (glutathione-S-transferase and nonspecific esterase) in the gut and fat body of the larvae from the Ordynsky District was 1.7–2.5 times that in the Vengerovsky insect group. The bacteria of the family Enterobacteriaceae and genus Citrobacter were found to be the dominant gut microbiota groups in both NSO districts, except for the larvae from the Ordynsky District, in which the major gut microbial groups included also the genus Spiroplasma. All insects studied did not differ in the level of sensitivity to B. thuringiensis. The development of bacterial infection in the gut of L. decemlineata from different NSO districts entailed a 2- to 3-fold increase in phenoloxidase activity in the hemolymph of insects from both districts, as well as a 1.5-fold increase in the total hemocyte count only in insects from the Ordynsky District. These findings demonstrate that insects of different geographical populations can effectively readjust their protective strategy against entomopathogens, balancing between the innate and induced resistance mechanisms.