Chemical entrapment and killing of insects by bacteria

Abstract Actinobacteria such as the filamentous streptomycetes are widely known for their ability to produce specialized metabolites that include antibacterial and antifungal compounds. In addition, a growing body of work demonstrates that many insects harbour actinobacteria on their bodies and in their nests. The result of these mutualistic relationships is the protection of their offspring or food sources by virtue of the bacterially encoded specialized metabolites. However, some actinobacteria produce molecules that are toxic to insects and the relevance of this toxicity in nature is unknown. We have explored interactions between streptomycetes and the fruit fly Drosophila. We find that many streptomycetes produce specialized metabolites that have potent larvicidal effects against the fly. Larvae that ingest spores of the species that produce these toxic molecules die as a result. Strikingly, the mechanism of toxicity is specific to the bacterium’s chemical arsenal: cosmomycin D producing cells induce a relatively slow-acting cell death-like response in the larval digestive tract and avermectin producing cells induce rapid onset, whole-body paralysis. We further show that fruit flies are attracted to the volatile terpene 2-methylisoborneol that is produced by most streptomycetes. This interaction can influence their food choice and egg-laying destination such that they preferentially deposit their eggs on contaminated food sources. As a result, the larvae that hatch in these toxic environments are subsequently killed. This phenomena of terpene-mediated attraction and specialized metabolite toxicity must pose a significant risk to insects in nature.