Host microbiome responses to the Snake Fungal Disease pathogen (Ophidiomyces ophidiicola) are driven by changes in microbial richness
Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287, 443–449 (2000).CAS
PubMed
ADS
Google Scholar
Pedersen, A. B., Jones, K. E., Nunn, C. L. & Altizer, S. Infectious diseases and extinction risk in wild mammals. Conserv. Biol. 21, 1269–1279 (2007).PubMed
PubMed Central
Google Scholar
Smith, K. F., Sax, D. F. & Lafferty, K. D. Evidence for the role of infectious disease in species extinction and endangerment. Conserv. Biol. 20, 1349–1357 (2006).PubMed
Google Scholar
Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).CAS
PubMed
ADS
Google Scholar
Paré, J. A. & Sigler, L. An overview of reptile fungal pathogens in the genera Nannizziopsis, Paranannizziopsis, and Ophidiomyces. J. Herpetol. Med. Surg. 26, 46–53 (2016).
Google Scholar
Warnecke, L. et al. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc. Natl. Acad. Sci. 109, 6999–7003 (2012).CAS
PubMed
PubMed Central
ADS
Google Scholar
Skerratt, L. F. et al. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125 (2007).
Google Scholar
Franklinos, L. H. V. et al. Emerging fungal pathogen Ophidiomyces ophiodiicola in wild European snakes. Sci. Rep. 7, 3844 (2017).PubMed
PubMed Central
ADS
Google Scholar
Lorch, J. M. et al. Snake fungal disease: an emerging threat to wild snakes. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150457 (2016).
Google Scholar
Bustos, M. L., Nicolás Sánchez, M., Peichoto, M. E. & Teibler, G. P. First report of fungal disease in a South American snake. Rev. Investig. Vet. Perú 29, 1036–1042 (2018).Sun, P.-L. et al. Infection with Nannizziopsis guarroi and Ophidiomyces ophiodiicola in reptiles in Taiwan. Transbound. Emerg. Dis. https://doi.org/10.1111/tbed.14049 (2021).Article
PubMed
Google Scholar
Haynes, E. et al. First report of ophidiomycosis in a free-ranging California kingsnake (Lampropeltis californiae) in California, USA. J. Wildl. Dis. 57, 246–249 (2021).CAS
PubMed
Google Scholar
Takami, Y. et al. First report of ophidiomycosis in Asia caused by Ophidiomyces ophiodiicola in captive snakes in Japan. J. Vet. Med. Sci. 83, 1234–1239 (2021).CAS
PubMed
PubMed Central
Google Scholar
Lorch, J. M. et al. Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease. MBio 6, e01534 (2015).CAS
PubMed
PubMed Central
Google Scholar
Koenig, J. E. et al. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. 108, 4578–4585 (2011).CAS
PubMed
ADS
Google Scholar
Huttenhower, C. et al. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).CAS
ADS
Google Scholar
Grice, E. A. & Segre, J. A. The skin microbiome. Nat. Rev. Microbiol. 9, 244–253 (2011).CAS
PubMed
PubMed Central
Google Scholar
Gall, C. A. et al. The bacterial microbiome of Dermacentor andersoni ticks influences pathogen susceptibility. ISME J. 10, 1846–1855 (2016).CAS
PubMed
PubMed Central
Google Scholar
Gould, A. L. et al. Microbiome interactions shape host fitness. Proc. Natl. Acad. Sci. 115, E11951–E11960 (2018).CAS
PubMed
PubMed Central
Google Scholar
Hanning, I. & Diaz-Sanchez, S. The functionality of the gastrointestinal microbiome in non-human animals. Microbiome 3, 51 (2015).PubMed
PubMed Central
Google Scholar
Jani, A. J. & Briggs, C. J. The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection. Proc. Natl. Acad. Sci. 111, E5049–E5058 (2014).CAS
PubMed
PubMed Central
ADS
Google Scholar
Walker, D. M. et al. Variability in snake skin microbial assemblages across spatial scales and disease states. ISME J. 13, 2209–2222 (2019).PubMed
PubMed Central
Google Scholar
Allender, M. C., Baker, S., Britton, M. & Kent, A. D. Snake fungal disease alters skin bacterial and fungal diversity in an endangered rattlesnake. Sci. Rep. 8, 12147 (2018).PubMed
PubMed Central
ADS
Google Scholar
Rykiel, E. J. Jr. Towards a definition of ecological disturbance. Aust. J. Ecol. 10, 361–365 (1985).
Google Scholar
Kong, H. H. et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 22, 850–859 (2012).CAS
PubMed
PubMed Central
Google Scholar
Ferrenberg, S. et al. Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME J. 7, 1102–1111 (2013).PubMed
PubMed Central
Google Scholar
Mackey, R. L. & Currie, D. J. The diversity–disturbance relationship: is it generally strong and peaked?. Ecology 82, 3479–3492 (2001).
Google Scholar
Connell, J. H. Diversity in tropical rain forests and coral reefs: high diversity of trees and corals is maintained only in a nonequilibrium state. Science 199, 1302–1310 (1978).CAS
PubMed
ADS
Google Scholar
Guthrie, A. L., Knowles, S., Ballmann, A. E. & Lorch, J. M. Detection of snake fungal disease due to Ophidiomyces ophiodiicola in Virginia, USA. J. Wildl. Dis. 52, 143–149 (2016).PubMed
Google Scholar
Chandler, H. C. et al. Ophidiomycosis prevalence in Georgia’s eastern indigo snake (Drymarchon couperi) populations. PLoS ONE 14, e0218351 (2019).CAS
PubMed
PubMed Central
Google Scholar
Tetzlaff, S. J. et al. Snake fungal disease affects behavior of free-ranging massasauga rattlesnakes (Sistrurus catenatus). Herpetol. Conserv. Biol. 12, 624–634 (2017).
Google Scholar
Lind, C. M., McCoy, C. M. & Farrell, T. M. Tracking outcomes of snake fungal disease in free-ranging pygmy rattlesnakes (Sistrurus miliarius). J. Wildl. Dis. 54, 352–356 (2018).PubMed
Google Scholar
Lind, C. M., Lorch, J. M., Moore, I. T., Vernasco, B. J. & Farrell, T. M. Seasonal sex steroids indicate reproductive costs associated with snake fungal disease. J. Zool. 307, 104–110 (2019).
Google Scholar
McKenzie, J. M. et al. Field diagnostics and seasonality of Ophidiomyces ophiodiicola in wild snake populations. EcoHealth 16, 141–150 (2019).PubMed
Google Scholar
McCoy, C. M., Lind, C. M. & Farrell, T. M. Environmental and physiological correlates of the severity of clinical signs of snake fungal disease in a population of pigmy rattlesnakes, Sistrurus miliarius. Conserv. Physiol. 5, cow077 (2017).Hill, A. J. et al. Common cutaneous bacteria isolated from snakes inhibit growth of Ophidiomyces ophiodiicola. EcoHealth 15, 109–120 (2018).PubMed
Google Scholar
Baker, S. et al. Case definition and diagnostic testing for Snake Fungal Disease. Herpetol. Rev. 50, 279–285 (2019).
Google Scholar
Chase, J. M., Kraft, N. J. B., Smith, K. G., Vellend, M. & Inouye, B. D. Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2, art24 (2011).Agugliaro, J., Lind, C. M., Lorch, J. M. & Farrell, T. M. An emerging fungal pathogen is associated with increased resting metabolic rate and total evaporative water loss rate in a winter-active snake. Funct. Ecol. 34, 486–496 (2020).
Google Scholar
Frick, W. F. et al. Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence. Ecology 98, 624–631 (2017).PubMed
Google Scholar
Gervasi, S. S., Hunt, E. G., Lowry, M. & Blaustein, A. R. Temporal patterns in immunity, infection load and disease susceptibility: understanding the drivers of host responses in the amphibian-chytrid fungus system. Funct. Ecol. 28, 569–578 (2014).
Google Scholar
Allender, M. C. et al. Development of snake fungal disease after experimental challenge with Ophidiomyces ophiodiicola in cottonmouths (Agkistrodon piscivorous). PLoS ONE 10, e0140193 (2015).PubMed
PubMed Central
Google Scholar
Briggs, C. J., Knapp, R. A. & Vredenburg, V. T. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl. Acad. Sci. 107, 9695–9700 (2010).CAS
PubMed
PubMed Central
ADS
Google Scholar
Neuman-Lee, L. A. et al. Assessing multiple endpoints of atrazine ingestion on gravid Northern Watersnakes (Nerodia sipedon) and their offspring. Environ. Toxicol. 29, 1072–1082 (2014).CAS
PubMed
ADS
Google Scholar
Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009).CAS
PubMed
ADS
Google Scholar
Kueneman, J. G. et al. Community richness of amphibian skin bacteria correlates with bioclimate at the global scale. Nat. Ecol. Evol. 3, 381–389 (2019).PubMed
Google Scholar
Manichanh, C. et al. Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55, 205–211 (2006).CAS
PubMed
PubMed Central
Google Scholar
Murphy, G. E. P. & Romanuk, T. N. A meta-analysis of declines in local species richness from human disturbances. Ecol. Evol. 4, 91–103 (2014).PubMed
Google Scholar
Jani, A. J. et al. The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance. ISME J. 15, 1628–1640 (2021).CAS
PubMed
PubMed Central
Google Scholar
Zaneveld, J. R., McMinds, R. & Vega Thurber, R. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2, 1–8 (2017).
Google Scholar
Anderson, M. J. et al. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol. Lett. 14, 19–28 (2011).PubMed
ADS
Google Scholar
Lankau, E. W., Hong, P.-Y. & Mackie, R. I. Ecological drift and local exposures drive enteric bacterial community differences within species of Galápagos iguanas. Mol. Ecol. 21, 1779–1788 (2012).PubMed
Google Scholar
Mebert, K. Good species despite massive hybridization: genetic research on the contact zone between the watersnakes Nerodia sipedon and N. fasciata in the Carolinas, USA. Mol. Ecol. 17, 1918–1929 (2008).CAS
PubMed
Google Scholar
Bohuski, E., Lorch, J. M., Griffin, K. M. & Blehert, D. S. TaqMan real-time polymerase chain reaction for detection of Ophidiomyces ophiodiicola, the fungus associated with snake fungal disease. BMC Vet. Res. 11, 95 (2015).PubMed
PubMed Central
Google Scholar
Wiens, J. A. Spatial scaling in ecology. Funct. Ecol. 3, 385–397 (1989).
Google Scholar
Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. 108, 4516–4522 (2011).CAS
PubMed
ADS
Google Scholar
Fadrosh, D. W. et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6 (2014).PubMed
PubMed Central
Google Scholar
Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).CAS
PubMed
PubMed Central
ADS
Google Scholar
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K. & Schloss, P. D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the Miseq Illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112–5120 (2013).CAS
PubMed
PubMed Central
ADS
Google Scholar
Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl. Acids Res. 41, D590–D596 (2013).CAS
PubMed
Google Scholar
Yilmaz, P. et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucl. Acids Res. 42, D643–D648 (2014).CAS
PubMed
Google Scholar
Weiss, S. et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5, 27 (2017).PubMed
PubMed Central
Google Scholar
R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2021).Bozdogan, H. Model selection and akaike’s information criterion (AIC): the general theory and its analytical extensions. Psychometrika 52, 345–370 (1987).MathSciNet
MATH
Google Scholar
Fox, J. & Weisberg, S. An R Companion to Applied Regression (SAGE Publications, Thousand Oaks, 2011).
Google Scholar
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).MATH
Google Scholar
Heip, C. A new index measuring evenness. J. Mar. Biol. Assoc. UK 54, 555–557 (1974).
Google Scholar More
