Skin bacterial community differences among three species of co-occurring Ranid frogs

Skin microbial communities are an essential part of host health and can play a role in mitigating disease. Host and environmental factors can shape and alter these microbial communities and, therefore, we need to understand to what extent these factors influence microbial communities and how this can impact disease dynamics. Microbial communities have been studied in amphibian systems due to skin microbial communities providing some resistance to the amphibian chytrid fungus, Batrachochytrium dendrobatidis. However, we are only starting to understand how host and environmental factors shape these communities for amphibians. In this study, we examined whether amphibian skin bacterial communities differ among host species, host infection status, host developmental stage, and host habitat. We collected skin swabs from tadpoles and adults of three Ranid frog species (Lithobates spp.) at the Mianus River Gorge Preserve in Bedford, New York, USA, and used 16S rRNA gene amplicon sequencing to determine bacterial community composition. Our analysis suggests amphibian skin bacterial communities change across host developmental stages, as has been documented previously. Additionally, we found that skin bacterial communities differed among Ranid species, with skin communities on the host species captured in streams or bogs differing from the communities of the species captured on land. Thus, habitat use of different species may drive differences in host-associated microbial communities for closely-related host species.

[1]  Yang Cao,et al.  microbiomeMarker: an R/Bioconductor package for microbiome marker identification and visualization , 2022, Bioinform..

[2]  C. Gieger,et al.  Host traits, lifestyle and environment are associated with human skin bacteria , 2021, The British journal of dermatology.

[3]  Cédric Arisdakessian,et al.  The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance , 2021, The ISME Journal.

[4]  Ariel Kruger.  Frog Skin Microbiota Vary With Host Species and Environment but Not Chytrid Infection , 2020, Frontiers in Microbiology.

[5]  E. Rebollar,et al.  The Amphibian Skin Microbiome and Its Protective Role Against Chytridiomycosis , 2020, Herpetologica.

[6]  J. Foster,et al.  Field trial of a probiotic bacteria to protect bats from white-nose syndrome , 2019, Scientific Reports.

[7]  R. Harris,et al.  Skin bacterial communities of neotropical treefrogs vary with local environmental conditions at the time of sampling , 2019, PeerJ.

[8]  Mark Wilkinson,et al.  Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity , 2019, Science.

[9]  K. Kohl,et al.  Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices , 2019, Proceedings of the Royal Society B.

[10]  M. W. McCoy,et al.  Comparative Analysis of Anuran Amphibian Skin Microbiomes Across Inland and Coastal Wetlands , 2018, Microbial Ecology.

[11]  S. Rovito,et al.  The Influence of Habitat and Phylogeny on the Skin Microbiome of Amphibians in Guatemala and Mexico , 2018, Microbial Ecology.

[12]  S. Rovito,et al.  The Influence of Habitat and Phylogeny on the Skin Microbiome of Amphibians in Guatemala and Mexico , 2018, Microbial Ecology.

[13]  Francesco Asnicar,et al.  QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data science , 2018 .

[14]  R. Harris,et al.  Probiotics as a tool for disease mitigation in wildlife: insights from food production and medicine , 2018, Annals of the New York Academy of Sciences.

[15]  V. McKenzie,et al.  Assessment of Bacterial Communities Associated With the Skin of Costa Rican Amphibians at La Selva Biological Station , 2018, Front. Microbiol..

[16]  V. McKenzie,et al.  Host‐associated bacterial community succession during amphibian development , 2018, Molecular ecology.

[17]  C. Briggs,et al.  Host and Aquatic Environment Shape the Amphibian Skin Microbiome but Effects on Downstream Resistance to the Pathogen Batrachochytrium dendrobatidis Are Variable , 2018, Front. Microbiol..

[18]  V. Vredenburg,et al.  Skin Microbiomes of California Terrestrial Salamanders Are Influenced by Habitat More Than Host Phylogeny , 2018, Front. Microbiol..

[19]  D. Lesbarrères,et al.  Environmental and Host Effects on Skin Bacterial Community Composition in Panamanian Frogs , 2018, Front. Microbiol..

[20]  Casper W. Berg,et al.  glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling , 2017, R J..

[21]  A. Catenazzi,et al.  Cutaneous bacteria, but not peptides, are associated with chytridiomycosis resistance in Peruvian marsupial frogs , 2017 .

[22]  Delong Meng,et al.  An Integrated Insight into the Relationship between Soil Microbial Community and Tobacco Bacterial Wilt Disease , 2017, Front. Microbiol..

[23]  K. Zamudio,et al.  Temperature variation, bacterial diversity and fungal infection dynamics in the amphibian skin , 2017, Molecular ecology.

[24]  L. K. Belden,et al.  Skin bacterial microbiome of a generalist Puerto Rican frog varies along elevation and land use gradients , 2017, PeerJ.

[25]  R. Harris,et al.  Host Ecology Rather Than Host Phylogeny Drives Amphibian Skin Microbial Community Structure in the Biodiversity Hotspot of Madagascar , 2017, Front. Microbiol..

[26]  S. Sommer,et al.  The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation , 2017, Biodiversity and Conservation.

[27]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[28]  R. Harris,et al.  Skin bacterial diversity of Panamanian frogs is associated with host susceptibility and presence of Batrachochytrium dendrobatidis , 2016, The ISME Journal.

[29]  R. Jensen,et al.  Panamanian frog species host unique skin bacterial communities , 2015, Front. Microbiol..

[30]  A. M. Kilpatrick,et al.  Bacteria Isolated from Bats Inhibit the Growth of Pseudogymnoascus destructans, the Causative Agent of White-Nose Syndrome , 2015, PloS one.

[31]  C. Briggs,et al.  The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection , 2014, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Jensen,et al.  Amphibian skin may select for rare environmental microbes , 2014, The ISME Journal.

[33]  R. Knight,et al.  The amphibian skin‐associated microbiome across species, space and life history stages , 2014, Molecular ecology.

[34]  R. Harris,et al.  Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. , 2013, Ecology letters.

[35]  J. Richardson,et al.  First survey for the amphibian chytrid fungus Batrachochytrium dendrobatidis in Connecticut (USA) finds widespread prevalence. , 2013, Diseases of aquatic organisms.

[36]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[37]  M. Blaser,et al.  The human microbiome: at the interface of health and disease , 2012, Nature Reviews Genetics.

[38]  R. Knight,et al.  Co-habiting amphibian species harbor unique skin bacterial communities in wild populations , 2011, The ISME Journal.

[39]  Gaël Varoquaux,et al.  Scikit-learn: Machine Learning in Python , 2011, J. Mach. Learn. Res..

[40]  R. Harris,et al.  Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa , 2010 .

[41]  M. Fisher,et al.  Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. , 2009, Annual review of microbiology.

[42]  R. Harris,et al.  The Bacterially Produced Metabolite Violacein Is Associated with Survival of Amphibians Infected with a Lethal Fungus , 2009, Applied and Environmental Microbiology.

[43]  R. Harris,et al.  Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus , 2009, The ISME Journal.

[44]  R. Alford,et al.  Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. , 2009, Diseases of aquatic organisms.

[45]  C. K. Dodd,et al.  Widespread occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in the southeastern USA. , 2008, Diseases of aquatic organisms.

[46]  R. Harris,et al.  Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa , 2007 .

[47]  K. Ritchie.  Regulation of microbial populations by coral surface mucus and mucus-associated bacteria , 2006 .

[48]  B. Young,et al.  Status and Trends of Amphibian Declines and Extinctions Worldwide , 2004, Science.

[49]  P. Daszak,et al.  A DNA-BASED ASSAY IDENTIFIES BATRACHOCHYTRIUM DENDROBATIDIS IN AMPHIBIANS , 2004, Journal of wildlife diseases.

[50]  D E Green,et al.  Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[51]  OUP accepted manuscript , 2021, FEMS Microbiology Ecology.

[52]  I. de Bruijn,et al.  Exploring fish microbial communities to mitigate emerging diseases in aquaculture. , 2018, FEMS microbiology ecology.

[53]  B. Tripathi,et al.  Microbiome Variation Across Amphibian Skin Regions: Implications for Chytridiomycosis Mitigation Efforts , 2015, Microbial Ecology.

[54]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[55]  R. Speare,et al.  Distribution of the amphibian chytrid Batrachochytrium dendrobatidis and keratin during tadpole development , 2004 .