Bacterial protection of beetle-fungus mutualism

Abstract

Host-microbe symbioses play a critical role in the evolution of biological diversity and complexity. In a notably intricate system, southern pine beetles use symbiotic fungi to help overcome host-tree defenses and to provide nutrition for their larvae. We show that this beetle-fungal mutualism is chemically mediated by a bacterially produced polyunsaturated peroxide. The molecule's selective toxicity toward the beetle's fungal antagonist, combined with the prevalence and localization of its bacterial source, indicates an insect-microbe association that is both mutualistic and coevolved. This unexpected finding in a well-studied system indicates that mutualistic associations between insects and antibiotic-producing bacteria are more common than currently recognized and that identifying their small-molecule mediators can provide a powerful search strategy for therapeutically useful antimicrobial compounds.

Fig. 1

(A) SEM micrograph of adult SPB showing the relative placement of the mycangia (arrow), which is used to transport EsA. (B) SEM micrograph from the SPB gallery showing the relative placement of the actinomycetous bacterium (ba), fungus (fu), and beetle larva (la). (C) Representative examples of pairwise bioassay challenges illustrating inhibition of the fungal antagonist Om (left), by a SPB symbiotic actinomycete (strain SPB074). In contrast the SPB’s fungal mutualist EsA is relatively resistant (right) (see SOM for more details). (D) The structure of mycangimycin containing a seven-conjugated double bond chain and a five-membered endoperoxide ring.