Comparative Analysis of Anuran Amphibian Skin Microbiomes Across Inland and Coastal Wetlands

Abstract

Amphibians host a community of microbes on their skin that helps resist infectious disease via the dual influence of anti-pathogenic microbial species and emergent community dynamics. Many frogs rely on freshwater habitats, but salinization is rapidly increasing saltwater concentrations in wetlands around the globe, increasing the likelihood that frogs will come into contact with salt-contaminated habitats. Currently, we know little about how increased salt exposure will affect the symbiotic relationship between the skin microbes and frog hosts. To better understand how salt exposure in a natural context affects the frog skin microbiome, we use Hyla cinerea, a North American treefrog species that can inhabit brackish wetlands, to explore three questions. First, we determine the extent that microbial communities in the environment and on frog skin are similar across populations. Second, we assess the microbial species richness and relative abundance on frogs from habitats with different salinity levels to determine how salinity affects the microbiome. Third, we test whether the relative abundances of putatively pathogen-resistant bacterial species differ between frogs from inland and coastal environments. We found that the frog microbiome is more similar among frogs than to the microbial communities found in surface water and soil, but there is overlap between frog skin and the environmental samples. Skin microbial community richness did not differ among populations, but the relative abundances of microbes were different across populations and salinities. We found no differences in the relative abundances of the anti-fungal bacteria Janthinobacterium lividum, the genus Pseudomonas, and Serratia marcescens, suggesting that environmental exposure to saltwater has a limited influence on these putatively beneficial bacterial taxa.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig.5
Fig. 6
Fig. 7

References

  1. 1.

    Bellard C, Leclerc C, Leroy B, Bakkenes M, Veloz S, Thuiller W, Courchamp F (2014) Vulnerability of biodiversity hotspots to global change. Glob Ecol Biogeogr 23:1376–1386

    Article  Google Scholar 

  2. 2.

    Grimm NB, Chapin III FS, Bierwagen B, Gonzalez P, Groffman PM, Luo Y, Melton F, Nadelhoffer K, Pairis A, Raymond PA (2013) The impacts of climate change on ecosystem structure and function. Front Ecol Environ 11:474–482

    Article  Google Scholar 

  3. 3.

    Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends Ecol Evol 25:325–331. https://doi.org/10.1016/j.tree.2010.03.002

    Article  PubMed  Google Scholar 

  4. 4.

    Blois JL, Zarnetske PL, Fitzpatrick MC, Finnegan S (2013) Climate change and the past, present, and future of biotic interactions. Science 341:499–504. https://doi.org/10.1126/science.1237184

    Article  CAS  PubMed  Google Scholar 

  5. 5.

    Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884

    Article  CAS  PubMed  Google Scholar 

  6. 6.

    Kikuchi Y, Tada A, Musolin DL, Hari N, Hosokawa T, Fujisaki K, Fukatsu T (2016) Collapse of insect gut symbiosis under simulated climate change. MBio 7(5):e01578–16

  7. 7.

    Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:259–262

    Article  Google Scholar 

  8. 8.

    Lillywhite HB, Maderson PF (1988) The structure and permeability of integument. Am Zool 28:945–962

    Article  Google Scholar 

  9. 9.

    Lillywhite HB (2006) Water relations of tetrapod integument. J Exp Biol 209:202–226. https://doi.org/10.1242/jeb.02007

    Article  PubMed  Google Scholar 

  10. 10.

    Duellman WE, Trueb L (1994) Biology of amphibians. McGraw-Hill, New York, pp 670

  11. 11.

    Grice E, Segre J (2011) The skin microbiome. Nat Rev Microbiol 9:244–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Woodhams DC, Ardipradja K, Alford RA, Marantelli G, Reinert LK, Rollins-Smith LA (2007) Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim Conserv 10:409–417

    Article  Google Scholar 

  13. 13.

    Walke JB, Belden LK (2016) Harnessing the microbiome to prevent fungal infections: lessons from amphibians. PLoS Pathog 12:e1005796. https://doi.org/10.1371/journal.ppat.1005796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MP, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Sanchez-Azofeifa GA, Still CJ, Young BE (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167. https://doi.org/10.1038/nature04246

    Article  CAS  PubMed  Google Scholar 

  15. 15.

    Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci 95:9031–9036

    Article  CAS  PubMed  Google Scholar 

  16. 16.

    Kilpatrick AM, Briggs CJ, Daszak P (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol 25(2):109–118

    Article  PubMed  Google Scholar 

  17. 17.

    Lips KR (2016) Overview of chytrid emergence and impacts on amphibians. Philos Trans R Soc B 371(1709):20150465

    Article  Google Scholar 

  18. 18.

    Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR, Flaherty DC, Lam BA, Woodhams DC, Briggs CJ, Vredenburg VT, Minbiole KP (2009) Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 3:818–824

    Article  CAS  PubMed  Google Scholar 

  19. 19.

    Becker MH, Brucker RM, Schwantes CR, Harris RN, Minbiole KP (2009) The bacterially produced metabolite violacein is associated with survival of amphibians infected with a lethal fungus. Appl Environ Microbiol 75:6635–6638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Becker MH, Walke JB, Cikanek S, Savage AE, Mattheus N, Santiago CN, Minbiole KPC, Harris RN, Belden LK, Gratwicke B (2014) Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus. Proc R Soc Lond B Biol Sci 282:20142881. https://doi.org/10.1098/rspb.2014.2881

    Article  CAS  Google Scholar 

  21. 21.

    Woodhams DC, Alford RA, Antwis RE, Archer H, Becker MH, Belden LK, Bell SC, Bletz M, Daskin JH, Davis LR, Flechas SV (2015) Antifungal isolates database of amphibian skin-associated bacteria and function against emerging fungal pathogens. Ecology 96:595–595

    Article  Google Scholar 

  22. 22.

    Loudon AH, Holland JA, Umile TP, Burzynski EA, Minbiole KP, Harris RN (2014) Interactions between amphibians’ symbiotic bacteria cause the production of emergent anti-fungal metabolites. Front Microbiol 4:441

    Google Scholar 

  23. 23.

    Matos A, K L, Garland J (2005) Effects of microbial community diversity on the survival of Pseudomonas aeruginosa in the wheat rhizosphere. Microb Ecol 49:257–264

    Article  CAS  PubMed  Google Scholar 

  24. 24.

    Dillon R, Vennard C, Buckling A (2005) Diversity of locust gut bacteria protects against pathogen invasion. Ecol Lett 8:1291–1298

    Article  Google Scholar 

  25. 25.

    Belden LK, Harris RN (2007) Infectious diseases in wildlife: the community ecology context. Front Ecol Environ 5:533–539

    Article  Google Scholar 

  26. 26.

    Theriot CM, Koenigsknecht MJ, Carlson Jr PE, Hatton GE, Nelson AM, Li B, Huffnagle GB, Li JZ, Young VB, Nature communications (2014) Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 5. https://doi.org/10.1038/ncomms4114

  27. 27.

    Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM, Sonnenburg JL (2013) Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502:96–99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Loudon AH, Woodhams DC, Parfrey LW, Archer H, Knight R, McKenzie V, Harris RN (2014) Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). ISME J 8:830–840

    Article  CAS  PubMed  Google Scholar 

  29. 29.

    Walke JB, Harris RN, Reinert LK, Rollins-Smith LA, Woodhams DC (2011) Social immunity in amphibians: evidence for vertical transmission of innate defenses. Biotropica 43:396–400

    Article  Google Scholar 

  30. 30.

    Rebollar EA, Simonetti SJ, Shoemaker WR, Harris RN (2016) Direct and indirect horizontal transmission of the antifungal probiotic bacterium Janthinobacterium lividum on green frog (Lithobates clamitans) tadpoles. Appl Environ Microbiol 82:2457–2466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Lam BA, Walke JB, Vredenburg VT, Harris RNBC (2010) Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biol Conserv 143(2):529–531

    Article  Google Scholar 

  32. 32.

    Bell G (2001) Neutral macroecology. Science 293:2413–2418

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Huisman J, Weissing F (1999) Biodiversity of plankton by species oscillations and chaos. Nature 402:407–410

    Article  Google Scholar 

  34. 34.

    Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410

    Article  PubMed  Google Scholar 

  35. 35.

    Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci U S A 101:10854–10861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Loudon A, Venkataraman A, Van Treuren W, Woodhams D, Parfrey L, McKenzie V, Knight R, Schmidt T, Harris R (2016) Vertebrate hosts as islands: dynamics of selection, immigration, loss, persistence, and potential function of bacteria on salamander skin. Front Microbiol 7:.333

  37. 37.

    Belden LK, Hughey MC, Rebollar EA, Umile TP, Loftus SC, Burzynski EA, Minbiole KP, House LL, Jensen RV, Becker MH, Walke JB (2014) Panamanian frog species host unique skin bacterial communities. Front Microbiol 8:1171–1171

    Google Scholar 

  38. 38.

    Hughey MC, Walke JB, Becker MH, Umile TP, Burzynski EA, Minbiole KP, Iannetta AA, Santiago CN, Hopkins WA, Belden LK (2016) Short-term exposure to coal combustion waste has little impact on the skin microbiome of adult spring peepers (Pseudacris crucifer). Appl Environ Microbiol 82:3493–3502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Kueneman JG, Parfrey LW, Woodhams DC, Archer HM, Knight R, McKenzie VJ (2014) The amphibian skin-associated microbiome across species, space and life history stages. Mol Ecol 23:1238–1250

    Article  PubMed  Google Scholar 

  40. 40.

    Lillywhite HB, Licht P (1975) A comparative study of integumentary mucous secretions in amphibians. Comp Biochem Physiol A Physiol 51:937–941. https://doi.org/10.1016/0300-9629(75)90077-8

    Article  CAS  Google Scholar 

  41. 41.

    Diamond JM (1978) Niche shifts and the rediscovery of interspecific competition. Am Sci 66:322–331

    Google Scholar 

  42. 42.

    Tokeshi M (1993) Species abundance patterns and community structure. Adv Ecol Res 24:112–186

    Google Scholar 

  43. 43.

    Munday P (2004) Competitive coexistence of coral-dwelling fishes: the lottery hypothesis revisited. Ecology 85:623–628

    Article  Google Scholar 

  44. 44.

    Levy J (2000) The effects of antibiotic use on gastrointestinal function. Am J Gastroenterol 95:S8–S10

    Article  CAS  PubMed  Google Scholar 

  45. 45.

    Schmidt VT, Smith KF, Melvin DW, Amaral-Zettler LA (2015) Community assembly of a euryhaline fish microbiome during salinity acclimation. Mol Ecol 24(10):2537–2550

    Article  PubMed  Google Scholar 

  46. 46.

    Röthig T, Ochsenkühn MA, Roik A, van der Merwe R, Voolstra CR (2016) Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome. Mol Ecol 25:1308–1323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Herbert ER, Boon P, Burgin AJ, Neubauer SC, Franklin RB, Ardón M, Hopfensperger KN, Lamers LP, Gell P (2015) A global perspective on wetland salinization: ecological consequences of a growing threat to freshwater wetlands. Ecosphere 6:1–43

    Article  Google Scholar 

  49. 49.

    Williams SJ (2013) Sea level rise implications for coastal regions. J Coast Res 63:184–196. https://doi.org/10.2112/SI63-015.1

    Article  Google Scholar 

  50. 50.

    Mulligan RP, Walsh JP, Wadman HM (2012) Storm surge and surface waves in a large and shallow estuarine system during the passage of a hurricane. J Waterw Port Coast Ocean Eng 141(4):A5014001

  51. 51.

    Nicholls RJ, Cazenave A (2010) Sea-level rise and its impact on coastal zones. Science 328:1517–1520. https://doi.org/10.1126/science.1185782

    Article  CAS  PubMed  Google Scholar 

  52. 52.

    Ataie-Ashtiani B, Seyedabbasi MA (2006) Effects of sea-water intrusion interface on the flux of contaminant from coastal aquifers into the coastal water. J Coast Res 3:1654–1657

    Google Scholar 

  53. 53.

    Albecker MA, McCoy MW (2017) Adaptive responses to salinity stress across multiple life stages in anuran amphibians. Front Zool 14:40

    Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Hopkins GR, Brodie JED (2015) Occurrence of amphibians in saline habitats: a review and evolutionary perspective. Herpetol Monogr 29:1–27

    Article  Google Scholar 

  55. 55.

    Stockwell MP, Clulow J, Mahony MJ (2015) Evidence of a salt refuge: chytrid infection loads are suppressed in hosts exposed to salt. Oecologia 177:901–910

    Article  CAS  PubMed  Google Scholar 

  56. 56.

    Karraker NE, Ruthig GR (2009) Effect of road deicing salt on the susceptibility of amphibian embryos to infection by water molds. Environ Res 109:40–45

    Article  CAS  PubMed  Google Scholar 

  57. 57.

    Reavill DR (2001) Amphibian skin diseases. Vet Clin North Am Exot Anim Pract 4(2):413–440

  58. 58.

    Brown ME, Walls SC (2013) Variation in salinity tolerance among larval anurans: implications for community composition and the spread of an invasive, non-native species. Copeia 2013:543–551

    Article  Google Scholar 

  59. 59.

    Wilder AE, Welch AM (2014) Effects of salinity and pesticide on sperm activity and oviposition site selection in green treefrogs, Hyla cinerea. Copeia 2014:659–667

    Article  Google Scholar 

  60. 60.

    Brannelly L, Chatfield M, Richards-Zawacki C (2012) Field and laboratory studies of the susceptibility of the green treefrog (Hyla cinerea) to Batrachochytrium dendrobatidis infection. PLoS One 7:e38473. https://doi.org/10.1371/journal.pone.0038473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Green DE, Dodd CK (2007) Presence of amphibian chytrid fungus Batrachochytrium dendrobatidis and other amphibian pathogens at warm-water fish hatcheries in southeastern North America. Herpetol Conserv Biol 2:43–47

    Google Scholar 

  62. 62.

    Walke JB, Becker MH, Loftus SC, House LL, Cormier G, Jensen RV, Belden LK (2014) Amphibian skin may select for rare environmental microbes. ISME J 8:2207–2217. https://doi.org/10.1038/ismej.2014.77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. 64.

    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  Google Scholar 

  66. 66.

    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267

    Article  CAS  PubMed  Google Scholar 

  68. 68.

    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    Article  CAS  PubMed  Google Scholar 

  70. 70.

    R Core Development Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  71. 71.

    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2016) vegan: community ecology package

  72. 72.

    Wickham H (2007) Reshaping data with the reshape package. J Stat Softw 21(12):1–20

  73. 73.

    Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1(7):1–23

  74. 74.

    Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  75. 75.

    Ferrari SLP, Zeileis A (2010) Beta regression in R. J Stat Softw 34(2010):1–24

  76. 76.

    Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10

    Article  Google Scholar 

  77. 77.

    Preston FW (1960) Time and space and the variation of species. Ecology 41:1–27

    Article  Google Scholar 

  78. 78.

    Peet RK (1974) The measurement of species diversity. Annu Rev Ecol Syst 5:285–307

    Article  Google Scholar 

  79. 79.

    De Caceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference., CRAN

    Google Scholar 

  80. 80.

    Loudon AH, Holland JA, Umile TP, Burzynski EA, Minbiole KP, Harris RN (2014) Interactions between amphibians’ symbiotic bacteria cause the production of emergent anti-fungal metabolites. Front Microbiol 5:441

    Article  PubMed  PubMed Central  Google Scholar 

  81. 81.

    Woodhams DC, Rollins-Smith LA, Alford RA, Simon MA, Harris RN (2007) Innate immune defenses of amphibian skin: antimicrobial peptides and more. Anim Conserv 10:425–428

    Article  Google Scholar 

  82. 82.

    Becker MH, Harris RN, Minbiole KPC, Schwantes CR, Rollins-Smith LA, Reinert LK, Brucker RM, Domangue RJ, Gratwicke B (2011) Towards a better understanding of the use of probiotics for preventing chytridiomycosis in Panamanian golden frogs. Ecohealth 8:501–506

    Article  PubMed  Google Scholar 

  83. 83.

    Javaux EJ (2006) Extreme life on Earth—past, present, and possibly beyond. Res Microbiol 157:37–48

    Article  PubMed  Google Scholar 

  84. 84.

    Gonclaves G (2008) Herd immunity: recent uses in vaccine assessment. Expert Rev Vaccines 7:1493–1506

    Article  Google Scholar 

  85. 85.

    Bletz MC, Myers J, Woodhams DC, Rabemananjara FC, Rakotonirina A, Weldon C, Edmonds D, Vences M, Harris RN (2017) Estimating herd immunity to amphibian chytridiomycosis in Madagascar based on the defensive function of amphibian skin bacteria. Front Microbiol 8:1751

    Article  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Wright KM (1996) Amphibian husbandry and medicine. WB Saunders, Philadelphia

    Google Scholar 

  87. 87.

    Klaphake E (2009) Bacterial and parasitic diseases of amphibians. Vet Clin North Am Exot Anim Pract 12:597–608

    Article  PubMed  Google Scholar 

  88. 88.

    Rebollar EA, Gutiérrez-Preciado A, Noecker C, Eng A, Hughey MC, Medina D, Walke JB, Borenstein E, Jensen RV, Belden LK, Harris RN (2018) The skin microbiome of the neotropical frog Craugastor fitzingeri: inferring potential bacterial-host-pathogen interactions from metagenomic data. Front Microbiol 9:466

    Article  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Woodhams DC, Brandt H, Baumgartner S, Kielgast J, Küpfer E, Tobler U, Davis LR, Schmidt BR, Bel C, Hodel S, Knight R (2014) Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness. PLoS One 9:e96375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank members of the K. McCoy and M. McCoy lab groups at East Carolina University for thoughtful insights in the development of this project. We thank Laila Kirkpatrick at Virginia Tech for laboratory assistance as well as Zach Herbert and the staff at the Dana-Farber Cancer Institute’s Molecular Biology Core Lab at Harvard University for Illumina sequencing. Finally, we thank two anonymous reviewers whose reviews helped improve this manuscript.

Funding

Funding for this study was provided by the NSF grant DEB 1136640 awarded to Lisa Belden and the North Carolina Sea Grant (Project No. 2014-R/14-HCE-3) awarded to Michael W. McCoy and Molly A. Albecker.

Author information

Affiliations

Authors

Contributions

MA and MM conceived the study; MA and MM performed the field sampling; LB analyzed the samples; and MA, MM, and LB analyzed the data. MA, MM, and LB contributed to the writing of this manuscript.

Corresponding author

Correspondence to Molly A. Albecker.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Albecker, M.A., Belden, L.K. & McCoy, M.W. Comparative Analysis of Anuran Amphibian Skin Microbiomes Across Inland and Coastal Wetlands. Microb Ecol 78, 348–360 (2019). https://doi.org/10.1007/s00248-018-1295-9

Download citation

Keywords

  • Microbiome
  • Anuran amphibian
  • Frog
  • Mutualism
  • Skin
  • Pathogen resistance
  • Bacteria
  • Secondary salinization