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Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants

Ruchira Sen, Heather D. Ishak, Dora Estrada, Scot E. Dowd, Eunki Hong, and Ulrich G. Mueller
PNAS October 20, 2009 106 (42) 17805-17810; https://doi.org/10.1073/pnas.0904827106
Ruchira Sen
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Heather D. Ishak
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Dora Estrada
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Scot E. Dowd
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Eunki Hong
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Ulrich G. Mueller
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  1. Edited by Raghavendra Gadagkar, Indian Institute of Science, Bangalore, India, and approved August 14, 2009 (received for review May 1, 2009)

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Abstract

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 Pseudonocardia-Escovopsis coevolution model. Culture-dependent and culture-independent (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 garden-pathogenic 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

Footnotes

  • 1To whom correspondence should be addressed. E-mail: ruchira05{at}gmail.com or umueller{at}mail.utexas.edu
  • Author contributions: R.S., H.D.I., E.H., and U.G.M. designed research; R.S., H.D.I., D.E., S.E.D., E.H., and U.G.M. performed research; S.E.D. and U.G.M. contributed new reagents/analytic tools; R.S., H.D.I., S.E.D., and U.G.M. analyzed data; and R.S., H.D.I., and U.G.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. FJ948108–FJ948163, FJ985694–FJ985695, SRA008625.9).

  • See Commentary on page 17611.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0904827106/DCSupplemental.

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Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants
Ruchira Sen, Heather D. Ishak, Dora Estrada, Scot E. Dowd, Eunki Hong, Ulrich G. Mueller
Proceedings of the National Academy of Sciences Oct 2009, 106 (42) 17805-17810; DOI: 10.1073/pnas.0904827106

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Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants
Ruchira Sen, Heather D. Ishak, Dora Estrada, Scot E. Dowd, Eunki Hong, Ulrich G. Mueller
Proceedings of the National Academy of Sciences Oct 2009, 106 (42) 17805-17810; DOI: 10.1073/pnas.0904827106
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