Comparative genomics of dominant members of the gut core microbiome of the bark beetle, Dendroctonus rhizophagus (Curculionidae: Scolytinae) reveals potential functional complementarity in the detoxification process

Dendroctonus rhizophagus is a bark beetle of great forest importance, due to its aggressive root colonization of seedlings and young pine trees. To successfully complete their life cycle, these insects and associated microorganisms must overcome the trees’ complex defense system. However, little is known about the enzymes and metabolic pathways involved in xenobiotic detoxification by microbial symbionts of bark beetles. We investigated the genomic potential for detoxification in bacteria Acinetobacter, Pseudomonas, Rahnella and Serratia, as well as the yeasts Candida [Ogataea clade], Danielia, Cyberlindnera and Zygoascus, dominant members of the gut core microbiome of D. rhizophagus, through assembly, annotation, and comparison of their genomes. Genome analysis identified 1,293 genes in bacteria and yeasts related to 22 KO xenobiotic-degradation pathways. These pathways include those for aromatic compounds (benzoate, ferulate, vanillin), monoterpenes (pinene, camphor, geraniol, limonene) and diterpenes (dit genes). Additionally, the genomes contained genes encoding members of the following enzymatic families: cytochrome P450, carboxylesterases, laccases, aldehyde and alcohol dehydrogenases, flavin binding-monooxygenases, intradiol and extradiol dioxygenases, glutathione S-transferases, and multidrug resistance transporters (ABC, MFS, MATE, and RND) implicated in the detoxification process. Integration of these genes across the phases of xenobiotic detoxification reveals potential functional complementarity between bacteria and yeasts, suggesting that members of the gut microbiota of D. rhizophagus may enhance the beetle’s fitness by facilitating the metabolism and tolerance to the tree´s toxic compounds.