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

Bacillus thuringiensis-basedbiological insecticides are highly specific to various types ofinsects, while being considered environmentally safe. The Coloradopotato beetle Leptinotarsa decemlineata is oneof the most common insect pests of solanaceous crops worldwide.Its wide distribution across different climatic zones (i.e. highecological plasticity) and rapid development of the resistance todiverse chemical insecticides raise the question of the mechanismsunderlying these two fundamental properties of L.decemlineata. In this study, the indices of cell-mediatedand humoral immunity (phenoloxidase and antibacterial systems),activity of antioxidant and detoxification enzymes, gut microbiota,and susceptibility to B. thuringiensis bacteriawere studied in the larvae of L. decemlineata fromdifferent districts of the Novosibirsk Oblast (NSO). The total hemocytecount and lysozyme-like antibacterial activity in the hemolymphof insects from the Vengerovsky District were 1.5–2 times higherthan in the larvae from the Ordynsky District. The activity of detoxificationenzymes (glutathione-S-transferase and nonspecific esterase) inthe gut and fat body of the larvae from the Ordynsky District was1.7–2.5 times that in the Vengerovsky insect group. The bacteriaof the family Enterobacteriaceae andgenus Citrobacter were foundto be the dominant gut microbiota groups in both NSO districts,except for the larvae from the Ordynsky District, in which the majorgut microbial groups included also the genus Spiroplasma.All insects studied did not differ in the level of sensitivity to B. thuringiensis. The developmentof 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 ofinsects from both districts, as well as a 1.5-fold increase in thetotal hemocyte count only in insects from the Ordynsky District.These findings demonstrate that insects of different geographicalpopulations can effectively readjust their protective strategy againstentomopathogens, balancing between the innate and induced resistancemechanisms.