Abstract

Actinobacteria produce antibacterial and antifungal specialized metabolites. Many insects harbour actinobacteria on their bodies or in their nests and use these metabolites for protection. However, some actinobacteria produce metabolites that are toxic to insects and the evolutionary relevance of this toxicity is unknown. Here we explore chemical interactions between streptomycetes and the fruit fly Drosophila melanogaster. We find that many streptomycetes produce specialized metabolites that have potent larvicidal effects against the fly; larvae that ingest spores of these species die. The mechanism of toxicity is specific to the bacterium’s chemical arsenal: cosmomycin D producing bacteria induce a cell death-like response in the larval digestive tract; avermectin producing bacteria induce paralysis. Furthermore, low concentrations of volatile terpenes like 2-methylisoborneol that are produced by streptomycetes attract fruit flies such that they preferentially deposit their eggs on contaminated food sources. The resulting larvae are killed during growth and development. The phenomenon of volatile-mediated attraction and specialized metabolite toxicity suggests that some streptomycetes pose an evolutionary risk to insects in nature.

Highlights

  • Actinobacteria produce antibacterial and antifungal specialized metabolites

  • To compare the prevalence of specialized metabolites that act on prokaryotes, unicellular eukaryotes and multicellular eukaryotes we created small molecule extracts from 56 Streptomyces strains and tested them for inhibitory activity against Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Candida albicans and Drosophila melanogaster

  • Focusing first on the microbial screens (Fig. 1a) we assessed the ability of extracts to inhibit >90% growth and found that 25 extracts were active against B. subtilis, two were active against E. coli, 8 were active against S. cerevisiae and 5 were active against C. albicans

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Summary

Introduction

Actinobacteria produce antibacterial and antifungal specialized metabolites. Many insects harbour actinobacteria on their bodies or in their nests and use these metabolites for protection. The phenomenon of volatile-mediated attraction and specialized metabolite toxicity suggests that some streptomycetes pose an evolutionary risk to insects in nature. Many actinomycetes have intimate contact with insects and other multicellular organisms[15] They have been identified in the microbiomes of fruit flies and other Diptera, honeybees, diamondback moths and silkworms[16,17,18,19]. This is perhaps not surprising as insects and streptomycetes are abundant, have co-existed for more than 479 million years, and are certain to have played important roles in each other’s evolutionary history[20]. This fungus is susceptible to a microfungal weed called

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