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Biotransformation of the Fungal Phytotoxin Fomannoxin by Soil Streptomycetes

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Abstract

Rhizosphere-associated Streptomyces sp. AcH 505 (AcH 505) promotes infection of Norway spruce (Picea abies) with the pathogenic fungus Heterobasidion abietinum 331, while Streptomyces sp. GB 4–2 (GB 4–2) enhances spruce defense against the fungus. To identify whether these bacteria influence the availability of the fungal phytotoxin fomannoxin and hence spruce infection, we analyzed the fomannoxin yield in H. abietinum 331-AcH 505 dual cultures. Further, the fate of fomannoxin was studied by adding the compound to cultures of AcH 505, GB 4–2 and nine other soil streptomycetes. Culture filtrates were extracted with ethyl acetate and analyzed by HPLC. Structures of novel compounds were elucidated by HPLC-HR-ESI-Orbitrap-MS and NMR spectroscopy. Phytotoxicity of the compounds was determined by in vivo measurement of maximum photosystem II efficiency of Arabidopsis thaliana seedlings. The amount of fomannoxin in H. abietinum 331-AcH 505 dual cultures was reduced compared to axenic fungus cultures and fungus-plant dual cultures. Following addition of fomannoxin to AcH 505 cultures, the compound disappeared and three novel fomannoxin derivatives without phytotoxic activity were detected. Another novel compound, fomannoxin amide, was discovered following fomannoxin addition to GB 4–2 cultures. Nine other streptomycetes converted fomannoxin into fomannoxin acid or fomannoxin amide. Both compounds exhibit the same phytotoxicity as fomannoxin. We, thus, conclude that the streptomycete-mediated modulation of spruce infection with H. abietinum 331 does not depend on the availability of fomannoxin. We further add evidence to the observation that the lipophilic side chain of fomannoxin is an important structural element for its phytotoxicity.

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Acknowledgments

We thank Mika Tarkka for critical reading of the manuscript, Margret Ecke and Andreas Kulik for technical assistance, and Sarah Mailänder for statistical analysis. This work has supported by the German Research Foundation (DFG, graduate school ‘Infection Biology’) and the Cluster of Excellence “Unifying Concepts in Catalysis” (DFG) coordinated by the Technical University Berlin.

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Authors and Affiliations

  1. IMIT, Universität Tübingen, Auf der Morgenstelle 1, 72076, Tübingen, Germany

    Nadine Horlacher, Rüdiger Hampp & Silvia D. Schrey

  2. IMIT, Universität Tübingen, Auf der Morgenstelle 28, 72076, Tübingen, Germany

    Nadine Horlacher, Dirk Schulz & Hans-Peter Fiedler

  3. Institut für Chemie, TU Berlin, Straße des 17. Juni 124, 10623, Berlin, Germany

    Jonny Nachtigall & Roderich D. Süssmuth

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  1. Nadine Horlacher
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Correspondence to Silvia D. Schrey.

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Horlacher, N., Nachtigall, J., Schulz, D. et al. Biotransformation of the Fungal Phytotoxin Fomannoxin by Soil Streptomycetes. J Chem Ecol 39, 931–941 (2013). https://doi.org/10.1007/s10886-013-0290-3

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