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Open Access Highly Accessed Research article

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

Jörg Barke1, Ryan F Seipke1, Sabine Grüschow2, Darren Heavens3, Nizar Drou3, Mervyn J Bibb4, Rebecca JM Goss2, Douglas W Yu15 and Matthew I Hutchings16*

Author Affiliations

1 School of Biological Sciences, University of East Anglia, Norwich, Norwich Research Park, NR4 7TJ, UK

2 School of Chemistry, University of East Anglia, Norwich, Norwich Research Park, NR4 7TJ, UK

3 The Genome Analysis Centre, Norwich, Norwich Research Park, NR4 7UH, UK

4 Department of Molecular Microbiology, John Innes Centre, Norwich, Norwich Research Park, NR4 7UH, UK

5 State Key Laboratory of Genetic Resources, and Evolution, Ecology, Conservation and Environment Center (ECEC), Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China

6 School of Medicine, Health Policy and Practice, University of East Anglia, Norwich, Norwich Research Park, NR4 7TJ, UK

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BMC Biology 2010, 8:109  doi:10.1186/1741-7007-8-109

Published: 26 August 2010

Abstract

Background

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. 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.

Results

In 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.

Conclusions

Our results show that a combination of co-evolution and environmental sampling results in the diversity of actinomycete symbionts and antibiotics associated with attine ants.