The nesting preference of an invasive ant is associated with the cues produced by actinobacteria in soil

Abstract

Soil-dwelling animals are at risk of pathogen infection in soils. When choosing nesting sites, animals could reduce this risk by avoiding contact with pathogens, yet there is currently little evidence. We tested this hypothesis using Solenopsis invicta as a model system. Newly mated queens of S. invicta were found to nest preferentially in soil containing more actinobacteria of Streptomyces and Nocardiopsis and to be attracted to two volatiles produced by these bacteria, geosmin and 2-methylisoborneol. Actinobacteria-rich soil was favored by S. invicta and this soil contained fewer putative entomopathogenic fungi than adjacent areas. Queens in such soil benefited from a higher survival rate. In culture, isolated actinobacteria inhibited entomopathogenic fungi, suggested that their presence may reduce the risk of fungal infection. These results indicated a soil-dwelling ant may choose nest sites presenting relatively low pathogen risk by detecting the odors produced by bacteria with anti-fungal properties.

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

“…The two metabolites attract Folsomia candida (springtails), which feed on Streptomyces colonies, where spores attach to their hydrophobic cuticles and are dispersed by the soil-dwelling hexapods to new and relatively distant locations [ 32 ]. 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 ].…”

Ammonia Production by Streptomyces Symbionts of Acromyrmex Leaf-Cutting Ants Strongly Inhibits the Fungal Pathogen Escovopsis

“…Studying the biological role of volatile compounds from Actinomycetes recently gained attention among researchers interested in the chemical ecology of Actinomycetes [ 35 , 36 , 37 ]. Huang et al revealed that Solenopsis invicta ants favor soils rich in Actinomyces bacteria by recognizing their characteristic volatiles, 2-methylisoborneol and geosmin [ 40 ]. In the context of leaf-cutting ants, Silva-Junior et al recently discovered that Actinomyces symbionts produce the same pyrazines [ 41 ] that the ants use as infochemicals [ 42 , 43 , 44 ].…”

The ubiquitous terpene geosmin is a warning chemical

“…The use of geosmin as an aposematic signal may explain its reported effects on other eukaryotes and its prevalence across a range of unrelated microbes. Geosmin attracts Solenopsis invicta because the terpene reliably indicates the presence of Streptomyces spp., and the toxic metabolites produced by these bacteria protect ant colonies from fungal infections 15 . Similarly, geosmin discourages egg laying by Drosophila, whose young are susceptible to bacterial toxins 14 , while also signalling the presence of edible cyanobacteria to the more toxin-resistant A. aegypti 8,42 .…”

“…The breadth of geosmin producers and their varied ecological niches complicates assignment of the compound’s broader function. Geosmin repels egg-laying Drosophila melanogaster , which has a dedicated olfactory sensory neuron for geosmin detection 14 , and attracts mosquitos and ants 8,15 , Geosmin attracts springtails to sporulating Streptomyces colonies, which then eat the bacteria and help disperse bacterial spores 16 , but this interaction would be of limited utility in aquatic environments 12 . Due to differing primary nutrient sources, life cycles, cell wall structures, predators, and symbionts the principal geosmin producers have few features in common 9,10,12 , but all produce a wealth of non-geosmin secondary metabolites 17 .…”