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Antifungal activity of different Xenorhabdus and Photorhabdus species against various fungal phytopathogens and identification of the antifungal compounds from X. szentirmaii

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Abstract

Xenorhabdus and Photorhabdus spp. are enteric bacterial symbionts of Steinernema and Heterorhabditis nematodes, respectively. These bacteria produce an extensive set of natural products (NPs) with antibacterial, antifungal, antiprotozoal, insecticidal, or other bioactivities when vectored into insect hemocoel by nematodes. We assessed the in vitro activity of different Xenorhabdus and Photorhabdus cell-free supernatants against important fungal phytopathogens, viz., Cryphonectria parasitica, Fusarium oxysporum, Rhizoctonia solani, and Sclerotinia sclerotiorum and identified the bioactive antifungal compound/s present in the most effective bacterial supernatant using the easyPACId (easy promoter–activated compound identification) approach against chestnut blight C. parasitica. Our data showed that supernatants from Xenorhabdus species were comparatively more effective than extracts from Photorhabdus in suppressing the fungal pathogens; among the bacteria assessed, Xenorhabdus szentirmaii was the most effective species against all tested phytopathogens especially against C. parasitica. Subsequent analysis revealed fabclavines as antifungal bioactive compounds in X. szentirmaii, generated by a polyketide synthase (PKS) and non-ribosomal peptide synthetase (NRPS) hybrid system. Fabclavines are broad-spectrum, heat-stable NPs that have great potential as biological control compounds against fungal plant pathogens. More studies are needed to assess the potential phytotoxicity of these compounds and their effects on non-target organisms before commercialization.

Key points

• Chemical fungicides have toxic effects on humans and other non-target organisms.

• Alternatives with novel modes of action to supplant current fungicide are needed.

• A novel bioactive antifungal compound from Xenorhabdus szentirmaii was identified.

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All the data generated from this study are included in this article.

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Funding

The study was supported by Aydin Adnan Menderes University Research Fund, Turkey (Project number: FEF-16003). Work in the Bode lab was supported in part by the LOEWE center TBG and the LOEWE research cluster MegaSyn.

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Authors and Affiliations

  1. Department of Biology, Faculty of Arts and Science, Aydin Adnan Menderes University, Aydin, Turkey

    Harun Cimen, Mustapha Touray, Sebnem Hazal Gulsen & Selcuk Hazir

  2. Department of Plant Protection, Faculty of Agriculture, Aydin Adnan Menderes University, Aydin, Turkey

    Omer Erincik

  3. Molecular Biotechnology, Department of Biosciences, Goethe Universität Frankfurt, Max-von-Laue-Str. 9, D-60438, Frankfurt am Main, Germany

    Sebastian L. Wenski & Helge B. Bode

  4. Senckenberg Gesellschaft für Naturforschung, 60325, Frankfurt am Main, Germany

    Helge B. Bode

  5. Buchmann Institute for Molecular Life Sciences (BMLS), Johann Wolfgang Goethe University, Max-von-Laue-Straße 15, 60438, Frankfurt am Main, Germany

    Helge B. Bode

  6. Max-Planck-Institute for Terrestrial Microbiology, Department of Natural Products in Organismic Interactions, 35043, Marburg, Germany

    Helge B. Bode

  7. USDA-ARS, Southeastern Fruit and Tree Nut Research Station, Byron, GA, 31008, USA

    David Shapiro-Ilan

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  1. Harun Cimen
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  2. Mustapha Touray
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  3. Sebnem Hazal Gulsen
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  4. Omer Erincik
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  5. Sebastian L. Wenski
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  6. Helge B. Bode
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  7. David Shapiro-Ilan
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  8. Selcuk Hazir
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Contributions

HC, SH, and DS designed the research. HC carried out the research. HB and SW generated promoter exchanged mutant strains. MT, SHG, and OE assisted with the experiments. HC, SH, and DS wrote the manuscript.

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Correspondence to Harun Cimen.

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Cimen, H., Touray, M., Gulsen, S.H. et al. Antifungal activity of different Xenorhabdus and Photorhabdus species against various fungal phytopathogens and identification of the antifungal compounds from X. szentirmaii. Appl Microbiol Biotechnol 105, 5517–5528 (2021). https://doi.org/10.1007/s00253-021-11435-3

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  • DOI: https://doi.org/10.1007/s00253-021-11435-3

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