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Common Cutaneous Bacteria Isolated from Snakes Inhibit Growth of Ophidiomyces ophiodiicola

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Abstract

There is increasing concern regarding potential impacts of snake fungal disease (SFD), caused by Ophidiomyces ophiodiicola (Oo), on free-ranging snake populations in the eastern USA. The snake cutaneous microbiome likely serves as the first line of defense against Oo and other pathogens; however, little is known about microbial associations in snakes. The objective of this study was to better define the composition and immune function of the snake cutaneous microbiome. Eight timber rattlesnakes (Crotalus horridus) and four black racers (Coluber constrictor) were captured in Arkansas and Tennessee, with some snakes exhibiting signs of SFD. Oo was detected through real-time qPCR in five snakes. Additional histopathological techniques confirmed a diagnosis of SFD in one racer, the species’ first confirmed case of SFD in Tennessee. Fifty-eight bacterial and five fungal strains were isolated from skin swabs and identified with Sanger sequencing. Non-metric multidimensional scaling and PERMANOVA analyses indicated that the culturable microbiome does not differ between snake species. Fifteen bacterial strains isolated from rattlesnakes and a single strain isolated from a racer inhibited growth of Oo in vitro. Results shed light on the culturable cutaneous microbiome of snakes and probiotic members that may play a role in fighting an emergent disease.

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Acknowledgements

The authors would like to thank Hannah Carroll, John Arnold, Calvin Hall, Dan Combs, and Vince Cobb for their contributions to field and laboratory work, and the two anonymous reviewers for their helpful comments.

Funding

Funding was provided by the Tennessee Wildlife Resources Agency, Grant 32801-00745, awarded to JEL and DMW, and by the US Fish and Wildlife Service, Multistate Wildlife Grant TN-U2-F14AP00077, Conserving Snake Species of Greatest Conservation Need Threatened by an Emerging Fungal Skin Disease, awarded to RDA.

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  1. Heather Fenton

    Present address: Environment and Natural Resources, Wildlife Division, Government of the Northwest Territories, Yellowknife, NT, Canada

Authors and Affiliations

  1. Department of Biology, Tennessee Technological University, 1100 North Dixie Avenue, Box 5063, Cookeville, TN, 38505, USA

    Aubree J. Hill, Jacob E. Leys, Fantasia M. Erdman, Katherine S. Malone, Gabrielle N. Russell, Roger D. Applegate & Donald M. Walker

  2. Biology Department, Cumberland University, Lebanon, TN, USA

    Danny Bryan

  3. Tennessee Wildlife Resources Agency, Nashville, TN, USA

    Roger D. Applegate

  4. Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, GA, USA

    Heather Fenton & Kevin Niedringhaus

  5. Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Champaign, IL, USA

    Andrew N. Miller

  6. Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Champaign, IL, USA

    Matthew C. Allender

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Contributions

Author’s Contribution

AJH and DMW conceived the experiment, AJH, DMW, MCA, and HF wrote the manuscript, JEL, DB, and RDA captured and sampled snakes, AJH, JEL, GNR, FME, KSM, HF, RDA, and KN collected data and analyzed results, ANM and MCA contributed fungal cultures. All authors contributed equally to the revision process of the manuscript.

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Correspondence to Aubree J. Hill.

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All applicable institutional and/or national guidelines for the care and use of animals were followed (Tennessee Technological University IACUC permit #15-16-001). Sample collection was permitted under TWRA #3886, TDEC #2016-026, and AK #020520155.

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Hill, A.J., Leys, J.E., Bryan, D. et al. Common Cutaneous Bacteria Isolated from Snakes Inhibit Growth of Ophidiomyces ophiodiicola . EcoHealth 15, 109–120 (2018). https://doi.org/10.1007/s10393-017-1289-y

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