Coevolution Between Attine Ants and Actinomycete Bacteria: A Reevaluation

Mueller, Ulrich G.; Dash, Debadutta; Rabeling, Christian; Rodrigues, André

doi:10.1111/j.1558-5646.2008.00501.x

Cited by 122 publications

(155 citation statements)

References 104 publications

(209 reference statements)

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“…Here we present microbiological and antibiotic evidence that contradict each of the above observations, adding to recent phylogenetic evidence that questioned the plausibility of Pseudonocardia-Escovopsis coevolution (17). Most importantly, Pseudonocardia of various attine species have nonspecific antibiotic properties that inhibit garden pathogens, endophytes, saprotrophs, arthropod pathogens, and most severely the ant-cultivated fungi.…”

mentioning

confidence: 57%

“…ammonioxydans) co-occurred in comparable proportions (Table S1). These 2 Pseudonocardia species, which belong to 2 distinct subgroups of Pseudonocardia (17), comprised almost 100% of all pseudonocardiaceous species, 60% of all actinomycetes, and 4.7% of all bacteria characterized for T. septentrionalis workers. In contrast, no such predominance of only 2 Pseudonocardia lineages occurred in the bacterial communities of Mycocepurus smithii and Cyphomyrmex wheeleri workers, where several distantly related Pseudonocardia species and other pseudonocardiaceous genera (e.g., Amycolatopsis) coexisted in significant abundance on workers (Table S1).…”

Section: Resultsmentioning

confidence: 99%

“…Many of the ant-associated Pseudonocardia species show antibiotic activity in vitro against Escovopsis (13)(14)(15). A diversity of actinomycete bacteria including Pseudonocardia also occur in the ant gardens, in the soil surrounding attine nests, and possibly in the substrate used by the ants for fungiculture (16,17).…”

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confidence: 99%

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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.

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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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mentioning

confidence: 57%

Section: Resultsmentioning

confidence: 99%

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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.

Self Cite

198

214

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“…A few studies have argued against the Pseudonocardia generic placement of the exosymbiotic Actinobacteria in fungus-growing ants (i.e. [40,41]). Kost et al [40] isolated 21 Actinobacteria strains from seven colonies of Acromyrmex octospinosus, two of which were identified as Streptomyces.…”

Section: Resultsmentioning

confidence: 99%

“…Kost et al [40] isolated 21 Actinobacteria strains from seven colonies of Acromyrmex octospinosus, two of which were identified as Streptomyces. Mueller et al [41] isolated diverse genera of Actinobacteria from fungus gardens and workers of 10 fungus-growing ant colonies and from infrabuccal pellets from incipient Atta texana queens. Contrary to the view of these authors, the isolation of other Actinobacteria genera from fungus-growing ants does not negate the presence of exosymbiotic Pseudonocardia from ant workers, especially in the cases where, as in the latter study, isolations were not conducted from worker cuticles.…”

Section: Resultsmentioning

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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