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Prodigiosin, Violacein, and Volatile Organic Compounds Produced by Widespread Cutaneous Bacteria of Amphibians Can Inhibit Two Batrachochytrium Fungal Pathogens

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Abstract

Symbiotic bacteria can produce secondary metabolites and volatile compounds that contribute to amphibian skin defense. Some of these symbionts have been used as probiotics to treat or prevent the emerging disease chytridiomycosis. We examined 20 amphibian cutaneous bacteria for the production of prodigiosin or violacein, brightly colored defense compounds that pigment the bacteria and have characteristic spectroscopic properties making them readily detectable, and evaluated the antifungal activity of these compounds. We detected violacein from all six isolates of Janthinobacterium lividum on frogs from the USA, Switzerland, and on captive frogs originally from Panama. We detected prodigiosin from five isolates of Serratia plymuthica or S. marcescens, but not from four isolates of S. fonticola or S. liquefaciens. All J. lividum isolates produced violacein when visibly purple, while prodigiosin was only detected on visibly red Serratia isolates. When applied to cultures of chytrid fungi Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal), prodigiosin caused significant growth inhibition, with minimal inhibitory concentrations (MIC) of 10 and 50 μM, respectively. Violacein showed a MIC of 15 μM against both fungi and was slightly more active against Bsal than Bd at lower concentrations. Although neither violacein nor prodigiosin showed aerosol activity and is not considered a volatile organic compound (VOC), J. lividum and several Serratia isolates did produce antifungal VOCs. White Serratia isolates with undetectable prodigiosin levels could still inhibit Bd growth indicating additional antifungal compounds in their chemical arsenals. Similarly, J. lividum can produce antifungal compounds such as indole-3-carboxaldehyde in addition to violacein, and isolates are not always purple, or turn purple under certain growth conditions. When Serratia isolates were grown in the presence of cell-free supernatant (CFS) from the fungi, CFS from Bd inhibited growth of the prodigiosin-producing isolates, perhaps indicative of an evolutionary arms race; Bsal CFS did not inhibit bacterial growth. In contrast, growth of one J. lividum isolate was facilitated by CFS from both fungi. Isolates that grow and continue to produce antifungal compounds in the presence of pathogens may represent promising probiotics for amphibians infected or at risk of chytridiomycosis. In a global analysis, 89% of tested Serratia isolates and 82% of J. lividum isolates were capable of inhibiting Bd and these have been reported from anurans and caudates from five continents, indicating their widespread distribution and potential for host benefit.

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Acknowledgements

We thank An Martel and Frank Pasmans for providing a Bsal culture. We thank Leyla Davis, Holly Archer, and Valerie McKenzie for providing bacterial isolates, Jordan Kueneman for contributing to database curation, and Carly Muletz for discussion of unpublished data. We thank Rebecca Dikow for assistance with genome assembly. Permits were provided by the Autoridad Nacional de Licencias Ambientales (01025).

Funding

This study was partly funded by the Dimensions in Biodiversity program DEB-1136662 to KPCM.

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Authors and Affiliations

  1. Biology Department, University of Massachusetts Boston, Boston, MA, 02125, USA

    Douglas C. Woodhams, Brandon C. LaBumbard, Kelly L. Barnhart & Molly C. Bletz

  2. Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, USA

    Matthew H. Becker & Brian Gratwicke

  3. Department of Biology and Chemistry, Liberty University, Lynchburg, VA, USA

    Matthew H. Becker

  4. Zoological Institute, Technische Universität Braunschweig, 38106, Braunschweig, Germany

    Molly C. Bletz & Miguel Vences

  5. School of Sciences, Pontificia Universidad Javeriana, Bogotá, AA 56710, Colombia

    Laura A. Escobar

  6. Department of Biological Sciences, Universidad de los Andes, Bogotá, AA 4976, Colombia

    Sandra V. Flechas

  7. Department of Chemistry, Villanova University, Villanova, PA, 19085, USA

    Megan E. Forman, Anthony A. Iannetta, Maureen D. Joyce & Kevin P. C. Minbiole

  8. Department of Chemistry, University of North Carolina, Chapel Hill, NC, 27514, USA

    Anthony A. Iannetta

  9. University of Antananarivo, Antananarivo, Madagascar

    Falitiana Rabemananjara

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  1. Douglas C. Woodhams
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Correspondence to Douglas C. Woodhams or Kevin P. C. Minbiole.

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Woodhams, D.C., LaBumbard, B.C., Barnhart, K.L. et al. Prodigiosin, Violacein, and Volatile Organic Compounds Produced by Widespread Cutaneous Bacteria of Amphibians Can Inhibit Two Batrachochytrium Fungal Pathogens. Microb Ecol 75, 1049–1062 (2018). https://doi.org/10.1007/s00248-017-1095-7

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