A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus

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.

Selvamicin, an atypical antifungal polyene from two alternative genomic contexts

“…A diglycosylated nystatin analog named NPP was isolated from Pseudonocardia autotrophica, although the additional sugar, an N-acetylglucosamine, is appended to the 4′ position of the mycosamine (14). A yet-unidentified nystatin analog from the ant-associated Pseudonocardia strain P1 also appears to have an additional sugar appendage at this same 4′ position (15). …”

Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants

“…For the fungus-growing ant Apterostigma dentigerum, Oh et al (12) reported the cyclodepsipeptide dentigerumycin from a Pseudonocardia symbiont with activity against E. weberi. From A. octospinosus, Barke et al (13) detected, besides the presence of the previously characterized candicidin polyene macrolide-producing Streptomyces (11), a Pseudonocardia symbiont that produces a nystatin-like polyene macrolide. These recent findings indicated that there are likely to be a number of diverse antifungal compounds yet to be identified from microbial symbionts of leaf-cutting/fungus-growing ants (11)(12)(13).…”

“…In addition to the characterization of microbial antifungal compounds (11)(12)(13) involved in mediating the interactions between the different partners, it has become evident that both a large number of pathogens (2-5) pose a threat to the ants' fungus garden and a large diversity of microbial symbionts can be found within the ants' nests. These symbionts fulfill diverse functions, including defense against pathogens or promotion of the growth of the garden fungus (e.g., by nitrogen fixation) (10)(11)(12)(13)(15)(16)(17). Because some bacterial symbionts of leaf-cutting ants can be also detrimental to the growth of the mutualistic fungus L. gongylophorus, the onesided view of leaf-cutting ants and Actinomyces symbionts as mutualistic partners of the leaf-cutting ants should be challenged (18).…”

Polyene macrolide biosynthesis in streptomycetes and related bacteria: recent advances from genome sequencing and experimental studies

“…Prolific producers have been found among symbionts of ants that culture and exploit fungal species (Haeder et al, 2009;Barke et al, 2010;Seipke et al, 2011a). Microbial genome sequencing is also contributing to discovery of new polyenes and to a more complete understanding of their biosynthesis.…”