Detoxification of conifer antimicrobial defenses promotes entomopathogenic fungus infection of bark beetles

In Norway spruce forests, complex interactions occur between Eurasian spruce bark beetles, the entomopathogenic fungus Beauveria bassiana, and the tree’s phenolic defenses. However, the role of spruce phenolics in this ecosystem remains unclear. We investigated the metabolism of phenolics by bark beetles and B. bassiana. Bark beetles hydrolyze spruce phenolic glycosides, producing antifungal aglycons. In response, B. bassiana, isolated from bark beetles, counter-adapts to this defense using a methylation-glycosylation pathway. This pathway, involving UDP-glycosyltransferase and O-methyltransferase, converts toxic phenolic aglycones into non-toxic methyl-glycosylated derivatives, enhancing their stability against hydrolysis. Functional knockout mutants confirmed the critical role of this pathway in fungal detoxification, development, and parasitization of bark beetles. This mechanism enhances B. bassiana’s ability to successfully infect bark beetles by counter-adapting to spruce-derived phenolics, providing a deeper understanding of the ecological interactions within this forest ecosystem.