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Abstract
BackgroundAttine ants live in an intensely studied tripartite mutualism with the fungus Leucoagaricus gongylophorus, which provides food to the ants, and with antibiotic-producing actinomycete bacteria. One hypothesis suggests that bacteria from the genus Pseudonocardia are the sole, co-evolved mutualists of attine ants and are transmitted vertically by the queens. A recent study identified a Pseudonocardia-produced antifungal, named dentigerumycin, associated with the lower attine Apterostigma dentigerum consistent with the idea that co-evolved Pseudonocardia make novel antibiotics. An alternative possibility is that attine ants sample actinomycete bacteria from the soil, selecting and maintaining those species that make useful antibiotics. Consistent with this idea, a Streptomyces species associated with the higher attine Acromyrmex octospinosus was recently shown to produce the well-known antifungal candicidin. Candicidin production is widespread in environmental isolates of Streptomyces, so this could either be an environmental contaminant or evidence of recruitment of useful actinomycetes from the environment. It should be noted that the two possibilities for actinomycete acquisition are not necessarily mutually exclusive.ResultsIn order to test these possibilities we isolated bacteria from a geographically distinct population of A. octospinosus and identified a candicidin-producing Streptomyces species, which suggests that they are common mutualists of attine ants, most probably recruited from the environment. We also identified a Pseudonocardia species in the same ant colony that produces an unusual polyene antifungal, providing evidence for co-evolution of Pseudonocardia with A. octospinosus.ConclusionsOur results show that a combination of co-evolution and environmental sampling results in the diversity of actinomycete symbionts and antibiotics associated with attine ants.
Highlights
Attine ants live in an intensely studied tripartite mutualism with the fungus Leucoagaricus gongylophorus, which provides food to the ants, and with antibiotic-producing actinomycete bacteria
All bacterial strains were screened in bioassays against a strain of Escovopsis weberi isolated from an A. octospinosus nest and against Candida albicans, a human pathogen
Bioassays revealed that strains P1, S3, S4, S5 and S9 inhibit the growth of E. weberi when grown on mannitol plus soya flour (MS) agar (Figure 2) while P1, S3, S4 and S5 inhibit the growth of C. albicans (Figure 3)
Summary
Attine ants live in an intensely studied tripartite mutualism with the fungus Leucoagaricus gongylophorus, which provides food to the ants, and with antibiotic-producing actinomycete bacteria. An alternative possibility is that attine ants sample actinomycete bacteria from the soil, selecting and maintaining those species that make useful antibiotics Consistent with this idea, a Streptomyces species associated with the higher attine Acromyrmex octospinosus was recently shown to produce the well-known antifungal candicidin. There is evidence that the fungal cultivar produces antibiotics in order to defend itself [7,8,9] and the ant workers defend their fungal gardens through a combination of grooming and weeding [8], production of their own antimicrobials through metapleural gland secretions [10] and the application of weedkillers. More recently, evidence has emerged that suggests attine ants are associated with bacteria from the actinomycete genera Streptomyces and Amycolatopsis and that antibiotic-producing actinomycetes can be horizontally acquired through male dispersal and sampling of actinomycetes from the soil [7,14]
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