Chemical entrapment and killing of insects by bacteria

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.

Production of Plant-Associated Volatiles by Select Model and Industrially Important Streptomyces spp.

“…A recent report has also shown that newly mated queens of Solenopsis invicta (red imported fire ant) are attracted by geosmin and 2-MIB to Streptomyces -rich locations for nesting, which have reduced levels of pathogenic fungi [ 36 ]. In addition, 2-MIB attracts Drosophila melanogaster (common fruit fly) for oviposition, where other Streptomyces specialized metabolites, such as cosmomycin D and avermectin, kill the larvae, providing a potential nutrient source for the Streptomyces [ 37 ]. Therefore, the Streptomyces use different VOCs for eliciting trans-kingdom interactions and for influencing biological outcomes, demonstrating the importance of such molecules in the environment.…”

Multikingdom interactions govern the microbiome in subterranean cultural heritage sites

“…First, interspecies mutualism can help the dispersal of microorganisms ( 15 ). Actinobacteria have been reported to release geosmin and 2-methylisoborneol, terpenoid substances which can attract soil-dwelling arthropods (e.g., springtails) as food sources and/or defensive symbionts ( 16 ) to help them disperse in fecal pellets and/or attach to bodies when arthropods move around ( 17 ). Such a dispersal mechanism could partly explain the dominance of Actinobacteria in ancient tombs and/or caves.…”

Analysis of Streptomyces Volatilomes Using Global Molecular Networking Reveals the Presence of Metabolites with Diverse Biological Activities

“…The exact reason for the production of plant-associated metabolites by Streptomyces is currently not clear, but since these bacteria inhabit the rhizosphere ( 125 ), it is possible that such metabolites (including VOCs) have roles in eliciting interactions with plants and other organisms in the environment ( 2 ). It was recently reported that certain Streptomyces strains produce VOCs to attract arthropods for the purposes of spore dispersal or to cause their killing for nutrient acquisition ( 23 , 24 ). In addition, some insects sense specific bacterial VOCs and are repelled by them as a possible mechanism of avoidance ( 25 , 26 ).…”

“…The VOCs geosmin and 2-methylisoborneol, which are responsible for the characteristic earthy odor of soil are also produced by Streptomyces and are thought to be involved in attracting invertebrates such as arthropods so that Streptomyces spores can adhere to them for dispersal ( 23 ). It has also been reported that fruit flies are attracted by low levels of 2-methylisoborneol produced by certain Streptomyces species, which then use another specialized metabolite to kill and utilize the flies, possibly for nutritional purposes ( 24 ). Concomitantly, some insects avoid geosmin and higher levels of 2-methylisoborneol, which possibly signal danger due to the presence of Streptomyces in the vicinity ( 25 , 26 ).…”