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

## TL;DR

A fungus that infects bark beetles detoxifies tree chemicals that normally protect the beetles from pathogens.

## Contribution

Discovery of a fungal detoxification pathway that allows Beauveria bassiana to overcome plant-derived antimicrobial defenses in bark beetles.

## Key findings

- Bark beetles convert tree phenolic compounds into more potent antimicrobial forms.
- Beauveria bassiana detoxifies these compounds via a two-step pathway involving glycosylation and methylation.
- Fungal strains lacking this pathway show reduced virulence against bark beetles.

## Abstract

Plants produce antimicrobial compounds to defend themselves against pathogens, and herbivorous insects may gain protection from their own pathogens by consuming these compounds. We found that bark beetles enzymatically convert some antimicrobial phenolic compounds of spruce trees into more potent antimicrobial derivatives. However, an insect-killing fungus counters these phenolic compounds with a two-step detoxification pathway to produce methylglucoside derivatives. Knocking out this fungal pathway by genetic transformation reduces the virulence of the fungus on bark beetles, proving the pathway’s importance for successful fungal infection.

After consumption by herbivores, plant antimicrobial defense compounds may enhance herbivore immunity to pathogenic microbes. In conifer-bark beetle interactions, beetles ingest large quantities of phloem tissue containing high concentrations of antimicrobial phenolic glucosides, such as stilbenes and flavonoids. It is not known, however, if these compounds increase bark beetle resistance to pathogens. We showed that Eurasian spruce bark beetles (Ips typographus) attacking Norway spruce (Picea abies) hydrolyze phenolic glucosides to their corresponding aglucones increasing their antifungal activity. However, the entomopathogen Beauveria bassiana, a natural fungal parasite of these beetles, detoxifies stilbene and flavonoid aglucones by forming methylglucoside derivatives. A two-step pathway involving a UDP-glycosyltransferase and an O-methyltransferase produces phenolic O-methylglucosides that are no longer toxic to B. bassiana and are stable to β-glucosidase action. Compared to wild-type strains of B. bassiana, mutant strains knocked out in the genes of this pathway exhibited decreased methylglucoside formation, slower growth on medium containing phenolic compounds, and reduced virulence toward bark beetles. Hence, methylglucosylation of plant-derived phenolics is a detoxification process that significantly increases the ability of B. bassiana to parasitize host insects consuming plant tissue high in phenolics, such as conifer phloem. This is one of the few examples of an entomopathogen that is able to resist the plant-derived defenses of an insect host.