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Non-specific association between filamentous bacteria and fungus-growing ants

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Abstract

Fungus-growing ants and their fungal cultivar form a highly evolved mutualism that is negatively affected by the specialized parasitic fungus Escovopsis. Filamentous Pseudonocardia bacteria occurring on the cuticle of attine ants have been proposed to form a mutualistic interaction with these ants in which they are vertically transmitted (i.e. from parent to offspring colonies). Given a strictly vertical transmission of Pseudonocardia, the evolutionary theory predicts a reduced genetic variability of symbionts among ant lineages. The aim of this study was to verify whether actinomycetes, which occur on Acromyrmex octospinosus leaf-cutting ants, meet this expectation by comparing their genotypic variability with restriction fragment length polymorphisms. Multiple actinomycete strains could be isolated from both individual ant workers and colonies (one to seven strains per colony). The colony specificity of actinomycete communities was high: Only 15% of all strains were isolated from more than one colony, and just 5% were present in both populations investigated. Partial sequencing of 16S ribosomal deoxyribonucleic acid of two of the isolated strains assigned both of them to the genus Streptomyces. Actinomycetes could also be isolated from workers of the two non-attine ant species Myrmica rugulosa and Lasius flavus. Sixty-two percent of the strains derived from attine ants and 80% of the strains isolated from non-attine ants inhibited the growth of Escovopsis. Our data suggest that the association between attine ants and their actinomycete symbionts is less specific then previously thought. Soil-dwelling actinomycetes may have been dynamically recruited from the environment (horizontal transmission), probably reflecting an adaptation to a diverse community of microbial pathogens.

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Acknowledgements

We thank Silvia Schmidt and Pascal Petronelli for invaluable help during fieldwork and Stefanie Bohnert for support in the laboratory. Constructive suggestions on the study and the manuscript by Anne Behrend, Hubert Herz, Michael Lakatos, Sandra Patiño, Silvia Schmidt, Dieter Spiteller and four anonymous referees are gratefully acknowledged. The Smithsonian Tropical Research Institute of the Republic of Panama assisted with the research and granted collecting permits. This work was supported by the European Large Scale Facility (‘Silvolab,’ French Guiana, no. DG/FJ/033/98) to Rainer Wirth. All experiments complied with the current laws in Germany, French Guiana and Panama.

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Authors and Affiliations

  1. Department of Plant Ecology and Systematics, Technical University of Kaiserslautern, Gottlieb-Daimler-Straße; Gebäude 13, 67663, Kaiserslautern, Germany

    Christian Kost, Tanja Lakatos, Wolf-Rüdiger Arendholz & Rainer Wirth

  2. Department of Genetics—Genome Research Unit, University of Kaiserslautern, Paul Ehrlich Straße 24, 67663, Kaiserslautern, Germany

    Christian Kost, Ingo Böttcher & Matthias Redenbach

  3. Department of Dermatology, University Mainz, Hautklinik, Langenbeckstr 1, 55131, Mainz, Germany

    Ingo Böttcher

  4. School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

    Christian Kost

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  1. Christian Kost
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  2. Tanja Lakatos
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  3. Ingo Böttcher
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Correspondence to Christian Kost.

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Kost, C., Lakatos, T., Böttcher, I. et al. Non-specific association between filamentous bacteria and fungus-growing ants. Naturwissenschaften 94, 821–828 (2007). https://doi.org/10.1007/s00114-007-0262-y

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  • DOI: https://doi.org/10.1007/s00114-007-0262-y

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