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Chemical Basis of the Synergism and Antagonism in Microbial Communities in the Nests of Leaf-Cutting Ants

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Chemical Basis of the Synergism and Antagonism in Microbial Communities in the Nests of Leaf-Cutting Ants Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants Ilka Schoeniana, Michael Spitellerb, Manoj Ghasteb, Rainer Wirthc, Hubert Herzd, and Dieter Spitellera,1 aDepartment of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany; bInstitute of Environmental Research of the Faculty of Chemistry, Dortmund University of Technology, D-44221 Dortmund, Germany; cDepartment of Plant Ecology and Systematics, Technical University of Kaiserslautern, D-67663 Kaiserslautern, Germany; and dSmithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancón, Republic of Panamá Edited* by Jerrold Meinwald, Cornell University, Ithaca, NY, and approved November 22, 2010 (received for review June 16, 2010) Leaf-cutting ants cultivate the fungus Leucoagaricus gongylo- pected that Pseudonocardia play a crucial role in the ants’ defense phorus, which serves as a major food source. This symbiosis is against pathogens. Although isolated microbial symbionts were threatened by microbial pathogens that can severely infect L. active against Escovopsis in the agar diffusion assay (10), until re- gongylophorus. Microbial symbionts of leaf-cutting ants, mainly cently, not a single compound from the ants’ microbial symbionts Pseudonocardia and Streptomyces, support the ants in defending had been characterized. Using bioassay-guided isolation, Haeder their fungus gardens against infections by supplying antimicrobial et al. (11) identified the antifungal candicidin macrolides that and antifungal compounds. The ecological role of microorganisms in are produced by a large number of Streptomyces symbionts isolated the nests of leaf-cutting ants can only be addressed in detail if their from three different leaf-cutting ant species (A. octospinosus, secondary metabolites are known. Here, we use an approach for the A. echinatior,andA. volcanus). For the fungus-growing ant Apter- rapid identification of established bioactive compounds from micro- ostigma dentigerum, Oh et al. (12) reported the cyclodepsipeptide organisms in ecological contexts by combining phylogenetic data, dentigerumycin from a Pseudonocardia symbiont with activity database searches, and liquid chromatography electrospray ionisa- against E. weberi. From A. octospinosus, Barke et al. (13) detected, tion high resolution mass spectrometry (LC-ESI-HR-MS) screening. besides the presence of the previously characterized candicidin – fi Antimycins A1 A4, valinomycins, and actinomycins were identi ed polyene macrolide-producing Streptomyces (11), a Pseudono- in this manner from Streptomyces symbionts of leaf-cutting ants. cardia symbiont that produces a nystatin-like polyene macrolide. Matrix-assisted laser desorption ionization (MALDI) imaging These recent findings indicated that there are likely to be a num- revealed the distribution of valinomycin directly on the integument ber of diverse antifungal compounds yet to be identified from of Acromyrmex echinatior workers. Valinomycins and actinomycins microbial symbionts of leaf-cutting/fungus-growing ants (11–13). fi were also directly identi ed in samples from the waste of A. echi- Over the last few years, researchers have realized that the eco- natior and A. niger leaf-cutting ants, suggesting that the compounds system of leaf-cutting ants is much more complex than initially exert their antimicrobial and antifungal potential in the nests of described as a coevolution of the leaf-cutting ants, their fungus leaf-cutting ants. Strong synergistic effects of the secondary meta- garden L. gongylophorus, one microbial symbiont (Pseudono- bolites produced by ant-associated Streptomyces were observed in cardia), and one specialized fungal pathogen (Escovopsis) (14). In the agar diffusion assay against Escovopsis weberi. Actinomycins addition to the characterization of microbial antifungal compounds strongly inhibit soil bacteria as well as other Streptomyces and Pseu- (11–13) involved in mediating the interactions between the differ- donocardia symbionts. The antifungal antimycins are not only active ent partners, it has become evident that both a large number of against pathogenic fungi but also the garden fungus L. gongylopho- pathogens (2–5) pose a threat to the ants’ fungus garden and rus itself. In conclusion, secondary metabolites of microbial sym- a large diversity of microbial symbionts can be found within the bionts of leaf-cutting ants contribute to shaping the microbial ants’ nests. These symbionts fulfill diverse functions, including de- communities within the nests of leaf-cutting ants. fense against pathogens or promotion of the growth of the garden fungus (e.g., by nitrogen fixation) (10–13, 15–17). Because some chemical imaging | antibiotics | chemical defense | ecological function bacterial symbionts of leaf-cutting ants can be also detrimental to the growth of the mutualistic fungus L. gongylophorus, the one- eaf-cutting/fungus-growing ants such as Acromyrmex are sided view of leaf-cutting ants and Actinomyces symbionts as mu- Lunique among ants, because they grow the fungus Leucoa- tualistic partners of the leaf-cutting ants should be challenged (18). garicus gongylophorus (Agaricales: Leucocoprineae) with har- In order to begin to better understand the ecological role of vested leaf material in chambers of their nests (1). In turn, microorganisms associated with leaf-cutting ants, it is crucial to L. gongylophorus is their major food source. However, this obli- expose the chemistry of the individual (micro)organisms in the gate mutualistic interaction is threatened by various microbial community. Extending phylogenetic comparisons of secondary pathogens such as the fungi Escovopsis (2, 3), Fusarium (4), Syn- metabolite producers (19–21), we used a combination of phylo- cephalastrum (4), and Trichoderma (4). In addition, microorganisms genetic analysis, database screening, and electrospray ionisation from the surrounding soil or plant pathogens accidentally in- high resolution mass spectrometry (ESI-HR-MS) analysis to troduced from harvested leaf material may compete with the garden fungus for nutrients and living space (5). Therefore, leaf- CHEMISTRY cutting ants treat their fungus gardens with great care, removing Author contributions: I.S. and D.S. designed research; I.S., M.S., M.G., R.W., H.H., and D.S. any suspicious material into waste chambers (6). Besides this performed research; I.S. and D.S. analyzed data; and I.S. and D.S. wrote the paper. mechanical cleaning behavior, leaf-cutting ants make use of an- The authors declare no conflict of interest. – timicrobial chemicals (7 9); these include 3-hydroxydecanoic *This Direct Submission article had a prearranged editor. ’ acid, which is secreted from the ants metapleural glands. Data deposition: The sequences reported in this paper have been deposited in the Gen- However, in 1999, Currie et al. (10) discovered microbial sym- Bank database (accession nos. HM538453 and HM538454). fi fi 1 bionts, identi ed as Pseudonocardia, from bio lms on the in- To whom correspondence should be addressed. E-mail: [email protected]. ECOLOGY tegument of leaf-cutting ants. Because Pseudonocardia belong to This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. the well-known antibiotic-producing Actinobacteria, it was sus- 1073/pnas.1008441108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1008441108 PNAS | February 1, 2011 | vol. 108 | no. 5 | 1955–1960 Downloaded by guest on September 24, 2021 rapidly identify ecologically relevant secondary metabolites from and Fig. S1). The identity of actinomycin D (1) and X2 (2) was microbial symbionts. In this way, we identified several antibiotics further confirmed by NMR and comparison with commercially and investigated their role in shaping the complex interactions in available actinomycin standards. Valinomycin (3) (28) and its the leaf-cutting ants’ ecosystem. closely related derivatives (29) were identified from the symbiont Streptomyces sp. Av25_3, revealing its high similarity to valino- Results mycin producers (Fig. 1, Table S1, and Fig. S1) such as S. anulatus Structure Elucidation of Antimicrobial and Antifungal Compounds (EU647474.1; 98.84%) (Table S1 and Fig. S1) and S. tsusimaensis from Microbial Symbionts. A variety of microbial symbionts from (EU622279; 99.21%) (Table S1 and Fig. S1) (20). Furthermore, three different Acromyrmex leaf-cutting ant species (A. octospi- we identified the well-known antifungal antimycins A1–A4 (4–7) nosus, A. echinatior, and A. volcanus) had been isolated in a pre- (30) (Fig. 1, Table S1, and Fig. S1), which are produced by mi- vious study. The symbiotic microorganisms were characterized crobial symbionts of Acromyrmex, on the basis of the high simi- using their 16S rDNA sequences for database comparison (11). larity of Streptomyces sp. Ao10 to S. albidoflavus (DQ855477.1; In addition, many more 16S rDNA sequences from microbial 99.72%) (Table S1 and Fig. S1). S. albidoflavus, which was re- symbionts of leaf-cutting ants are now available (11, 16, 22–24). cently isolated from mangroves, has been shown to produce However, because most research concerning the symbionts of antimycin A18 (31), suggesting the possible production of anti- leaf-cutting ants has focused on Pseudonocardia, their 16S rDNA mycins (4–7)byStreptomyces Ao10. sequences are the main ones that have been collected and used to The LC-MS screening of the extracts from all Streptomyces study the evolution of the symbiosis between Pseudonocardia
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