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Probiotics Modulate a Novel Amphibian Skin Defense Peptide That Is Antifungal and Facilitates Growth of Antifungal Bacteria

  • Douglas C. WoodhamsEmail author
  • Louise A. Rollins-Smith
  • Laura K. Reinert
  • Briana A. Lam
  • Reid N. Harris
  • Cheryl J. Briggs
  • Vance T. Vredenburg
  • Bhumi T. Patel
  • Richard M. Caprioli
  • Pierre Chaurand
  • Peter Hunziker
  • Laurent Bigler
Host Microbe Interactions

Abstract

Probiotics can ameliorate diseases of humans and wildlife, but the mechanisms remain unclear. Host responses to interventions that change their microbiota are largely uncharacterized. We applied a consortium of four natural antifungal bacteria to the skin of endangered Sierra Nevada yellow-legged frogs, Rana sierrae, before experimental exposure to the pathogenic fungus Batrachochytrium dendrobatidis (Bd). The probiotic microbes did not persist, nor did they protect hosts, and skin peptide sampling indicated immune modulation. We characterized a novel skin defense peptide brevinin-1Ma (FLPILAGLAANLVPKLICSITKKC) that was downregulated by the probiotic treatment. Brevinin-1Ma was tested against a range of amphibian skin cultures and found to inhibit growth of fungal pathogens Bd and B. salamandrivorans, but enhanced the growth of probiotic bacteria including Janthinobacterium lividum, Chryseobacterium ureilyticum, Serratia grimesii, and Pseudomonas sp. While commonly thought of as antimicrobial peptides, here brevinin-1Ma showed promicrobial function, facilitating microbial growth. Thus, skin exposure to probiotic bacterial cultures induced a shift in skin defense peptide profiles that appeared to act as an immune response functioning to regulate the microbiome. In addition to direct microbial antagonism, probiotic-host interactions may be a critical mechanism affecting disease resistance.

Keywords

Amphibian Antimicrobial peptide Chytridiomycosis Disease ecology Immune regulation Immunomodulation Microbiota Promicrobial 

Notes

Acknowledgements

We thank Tara Adiseshan for assistance with DGGE. This research was supported by a Sanofi Genzyme Undergraduate Research Fellowship to B.T.P., the U.S. National Science Foundation grant numbers 0640373 to R.N.H. and 1121758 to L.R-S., and the Swiss National Science Foundation grant number 31-125099 to D.C.W. with additional financial assistance from the Faculty of Science, University of Zurich.

Supplementary material

248_2019_1385_MOESM1_ESM.docx (258 kb)
ESM 1 (DOCX 257 kb)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Douglas C. Woodhams
    • 1
    Email author
  • Louise A. Rollins-Smith
    • 2
    • 3
  • Laura K. Reinert
    • 2
  • Briana A. Lam
    • 4
  • Reid N. Harris
    • 4
  • Cheryl J. Briggs
    • 5
  • Vance T. Vredenburg
    • 6
  • Bhumi T. Patel
    • 1
  • Richard M. Caprioli
    • 7
  • Pierre Chaurand
    • 8
  • Peter Hunziker
    • 9
  • Laurent Bigler
    • 10
  1. 1.Department of BiologyUniversity of Massachusetts BostonBostonUSA
  2. 2.Departments of Pathology, Microbiology and Immunology and PediatricsVanderbilt University School of MedicineNashvilleUSA
  3. 3.Department of Biological ScienceVanderbilt University School of MedicineNashvilleUSA
  4. 4.Department of BiologyJames Madison UniversityHarrisonburgUSA
  5. 5.Department of Ecology, Evolution, and Marine BiologyUniversity of CaliforniaSanta BarbaraUSA
  6. 6.Department of BiologySan Francisco State UniversitySan FranciscoUSA
  7. 7.Mass Spectrometry Research Center and Department of BiochemistryVanderbilt UniversityNashvilleUSA
  8. 8.Department of ChemistryUniversité de MontréalQCCanada
  9. 9.Functional Genomics Center ZurichUniversity of ZurichZurichSwitzerland
  10. 10.Department of ChemistryUniversity of ZurichZurichSwitzerland

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