Antonie van Leeuwenhoek

, Volume 98, Issue 2, pp 195–212 | Cite as

Placement of attine ant-associated Pseudonocardia in a global Pseudonocardia phylogeny (Pseudonocardiaceae, Actinomycetales): a test of two symbiont-association models

  • Ulrich G. Mueller
  • Heather Ishak
  • Jung C. Lee
  • Ruchira Sen
  • Robin R. Gutell
Original Paper

Abstract

We reconstruct the phylogenetic relationships within the bacterial genus Pseudonocardia to evaluate two models explaining how and why Pseudonocardia bacteria colonize the microbial communities on the integument of fungus-gardening ant species (Attini, Formicidae). The traditional Coevolution-Codivergence model views the integument-colonizing Pseudonocardia as mutualistic microbes that are largely vertically transmitted between ant generations and that supply antibiotics that specifically suppress the garden pathogen Escovopsis. The more recent Acquisition model views Pseudonocardia as part of a larger integumental microbe community that frequently colonizes the ant integument from environmental sources (e.g., soil, plant material). Under this latter model, ant-associated Pseudonocardia may have diverse ecological roles on the ant integument (possibly ranging from pathogenic, to commensal, to mutualistic) and are not necessarily related to Escovopsis suppression. We test distinct predictions of these two models regarding the phylogenetic proximity of ant-associated and environmental Pseudonocardia. We amassed 16S-rRNA gene sequence information for 87 attine-associated and 238 environmental Pseudonocardia, aligned the sequences with the help of RNA secondary structure modeling, and reconstructed phylogenetic relationships using a maximum-likelihood approach. We present 16S-rRNA secondary structure models of representative Pseudonocardia species to improve sequence alignments and identify sequencing errors. Our phylogenetic analyses reveal close affinities and even identical sequence matches between environmental Pseudonocardia and ant-associated Pseudonocardia, as well as nesting of environmental Pseudonocardia in subgroups that were previously thought to be specialized to associate only with attine ants. The great majority of ant-associated Pseudonocardia are closely related to autotrophic Pseudonocardia and are placed in a large subgroup of Pseudonocardia that is known essentially only from cultured isolates (rather than cloned 16S sequences). The preponderance of the known ant-associated Pseudonocardia in this latter clade of culturable lineages may not necessarily reflect abundance of these Pseudonocardia types on the ants, but isolation biases when screening for Pseudonocardia (e.g., preferential isolation of autotrophic Pseudonocardia with minimum-nutrient media). The accumulated phylogenetic patterns and the possibility of isolation biases in previous work further erode support for the traditional Coevolution-Codivergence model and calls for continued revision of our understanding how and why Pseudonocardia colonize the microbial communities on the integument of fungus-gardening ant species.

Keywords

Attine ant-microbe symbiosis Mutualism Antibiotic Secondary rRNA structure 

Notes

Acknowledgements

We thank Linquan Bai and Amanda Jones for the invitation to contribute to this special issue honoring Mike Goodfellow and his lifetime contribution to actinomycete ecology, systematics, and evolution. We thank Linda Kinkel, Liz Wellington, and Linquan Bai for the invitation to give a plenary talk at the 2009 ISBA Congress in Shanghai, for which we developed many ideas presented here. We thank two anonymous reviewers for constructive comments on the manuscript. The research was supported by NSF awards DEB-0919519, DEB-0639879, and DEB-0110073 to UGM; and NIH award R01GM067317 to RRG.

Supplementary material

10482_2010_9427_MOESM1_ESM.doc (5 mb)
Supplementary material 1 (DOC 5109 kb)

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Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Ulrich G. Mueller
    • 1
    • 3
  • Heather Ishak
    • 1
  • Jung C. Lee
    • 1
    • 2
    • 3
  • Ruchira Sen
    • 1
  • Robin R. Gutell
    • 1
    • 2
    • 3
  1. 1.Section of Integrative BiologyUniversity of Texas at AustinAustinUSA
  2. 2.Center for Computational Biology and BioinformaticsUniversity of Texas at AustinAustinUSA
  3. 3.Institute for Cellular and Molecular BiologyUniversity of Texas at AustinAustinUSA

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