Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis

Oh, Dong‐Chan; Poulsen, Michael; Currie, Cameron R.; Clardy, Jon

doi:10.1038/nchembio.159

Cited by 352 publications

(344 citation statements)

References 21 publications

(27 reference statements)

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“…To defend their fungal cultivar against Escovopsis sp., leaf-cutter ants use symbiotic actinobacteria of the genus Pseudonochardia that are housed in specialized cuticular structure on the ant's body (Caldera et al, 2009). These symbiotic bacteria produce the cyclic depsipeptide dentigerumycin that acts highly specific against Escovopsis sp., without harming the fungal cultivar (Oh et al, 2009). Thus, symbiotic bacteria are an integral part of antifungal immunity in a variety of organisms, offering an opportunity to resist fungal infection by a spread of bacterial symbionts.…”

Section: Discussionmentioning

confidence: 99%

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

et al. 2014

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Epithelial surfaces of most animals are colonized by diverse microbial communities. Although it is generally agreed that commensal bacteria can serve beneficial functions, the processes involved are poorly understood. Here we report that in the basal metazoan Hydra, ectodermal epithelial cells are covered with a multilayered glycocalyx that provides a habitat for a distinctive microbial community. Removing this epithelial microbiota results in lethal infection by the filamentous fungus Fusarium sp. Restoring the complex microbiota in gnotobiotic polyps prevents pathogen infection. Although mono-associations with distinct members of the microbiota fail to provide full protection, additive and synergistic interactions of commensal bacteria are contributing to full fungal resistance. Our results highlight the importance of resident microbiota diversity as a protective factor against pathogen infections. Besides revealing insights into the in vivo function of commensal microbes in Hydra, our findings indicate that interactions among commensal bacteria are essential to inhibit pathogen infection.

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Section: Discussionmentioning

confidence: 99%

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

et al. 2014

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“…Specialized activity of attine integumental Pseudonocardia only against Escovopsis (18) has been cited widely as evidence for (35) recently showed that attine actinomycetes inhibit endophytic fungi and Candida yeasts. In addition, Kost et al (36) showed that unidentified actinomycetes isolated from both attine and nonattine ants have comparable antibiotic activities.…”

Section: Discussionmentioning

confidence: 99%

Generalized antifungal activity and 454-screening ofPseudonocardiaandAmycolatopsisbacteria in nests of fungus-growing ants

Sen

Ishak

Estrada

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

197

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In many host-microbe mutualisms, hosts use beneficial metabolites supplied by microbial symbionts. Fungus-growing (attine) ants are thought to form such a mutualism with Pseudonocardia bacteria to derive antibiotics that specifically suppress the coevolving pathogen Escovopsis, which infects the ants' fungal gardens and reduces growth. Here we test 4 key assumptions of this PseudonocardiaEscovopsis coevolution model. Culture-dependent and cultureindependent (tag-encoded 454-pyrosequencing) surveys reveal that several Pseudonocardia species and occasionally Amycolatopsis (a close relative of Pseudonocardia) co-occur on workers from a single nest, contradicting the assumption of a single pseudonocardiaceous strain per nest. Pseudonocardia can occur on males, suggesting that Pseudonocardia could also be horizontally transmitted during mating. Pseudonocardia and Amycolatopsis secretions kill or strongly suppress ant-cultivated fungi, contradicting the previous finding of a growth-enhancing effect of Pseudonocardia on the cultivars. Attine ants therefore may harm their own cultivar if they apply pseudonocardiaceous secretions to actively growing gardens. Pseudonocardia and Amycolatopsis isolates also show nonspecific antifungal activities against saprotrophic, endophytic, entomopathogenic, and gardenpathogenic fungi, contrary to the original report of specific antibiosis against Escovopsis alone. We conclude that attine-associated pseudonocardiaceous bacteria do not exhibit derived antibiotic properties to specifically suppress Escovopsis. We evaluate hypotheses on nonadaptive and adaptive functions of attine integumental bacteria, and develop an alternate conceptual framework to replace the prevailing Pseudonocardia-Escovopsis coevolution model. If association with Pseudonocardia is adaptive to attine ants, alternate roles of such microbes could include the protection of ants or sanitation of the nest. mutualism ͉ symbiosis ͉ Attini ͉ Actinomycete ͉ Escovopsis

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“…In addition, the ants engage in a symbiotic association with Actinobacteria in the genus Pseudonocardia, which produce antibiotics that inhibit the growth of Escovopsis [20 -22]. Evidence supporting the role of Pseudonocardia in helping protect ant fungus gardens includes: (i) bioassays demonstrating bacterial inhibition of Escovopsis in vitro across most of the phylogenetic diversity of the association ( [20,22,23], this study); (ii) structural identification of a novel chemical compound responsible for inhibition of Escovopsis by an Apterostigma-associated Pseudonocardia symbiont [24]; (iii) two separate in vivo infection experiments in the fungus-growing ant genus Acromyrmex [21,22]; and (iv) the finding that experimental infections of Apterostigma colonies with a black yeast parasite of the ant bacterium association reduces the ability of Pseudonocardia to suppress Escovopsis and, consequently, defend the ant cultivar [25]. Support for a benefit to the bacteria by their ant hosts includes (i) the presence of morphological modifications in or on the cuticle of the majority of attine ant genera for maintaining the bacteria, and/or specialized cuticular glands that apparently secrete nutrients to support bacterial growth [23], and (ii) vertical transmission of Pseudonocardia bacteria to new colonies by prospective queens in several attine ant genera [20].…”

Section: Introductionmentioning

confidence: 99%

Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria

et al. 2010

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Fungus-growing ants (tribe Attini) engage in a mutualism with a fungus that serves as the ants' primary food source, but successful fungus cultivation is threatened by microfungal parasites (genus Escovopsis). Actinobacteria (genus Pseudonocardia) associate with most of the phylogenetic diversity of fungus-growing ants; are typically maintained on the cuticle of workers; and infection experiments, bioassay challenges and chemical analyses support a role of Pseudonocardia in defence against Escovopsis through antibiotic production. Here we generate a two-gene phylogeny for Pseudonocardia associated with 124 fungusgrowing ant colonies, evaluate patterns of ant -Pseudonocardia specificity and test Pseudonocardia antibiotic activity towards Escovopsis. We show that Pseudonocardia associated with fungus-growing ants are not monophyletic: the ants have acquired free-living strains over the evolutionary history of the association. Nevertheless, our analysis reveals a significant pattern of specificity between clades of Pseudonocardia and groups of related fungus-growing ants. Furthermore, antibiotic assays suggest that despite Escovopsis being generally susceptible to inhibition by diverse Actinobacteria, the ant-derived Pseudonocardia inhibit Escovopsis more strongly than they inhibit other fungi, and are better at inhibiting this pathogen than most environmental Pseudonocardia strains tested. Our findings support a model that many fungus-growing ants maintain specialized Pseudonocardia symbionts that help with garden defence.

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Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis

Cited by 352 publications

References 21 publications

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

Generalized antifungal activity and 454-screening ofPseudonocardiaandAmycolatopsisbacteria in nests of fungus-growing ants

Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria

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