The commensal skin microbiome of amphibian mountain populations and its association with the pathogen Batrachochytrium dendrobatidis.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
Oct 2024
Oct 2024
Historique:
received:
03
04
2024
accepted:
22
08
2024
medline:
8
10
2024
pubmed:
8
10
2024
entrez:
7
10
2024
Statut:
ppublish
Résumé
Microbial assemblages naturally living on the skin are an integral part of immunity. In amphibians, this skin microbiota may hold a mitigation solution against the fungal pathogen Batrachochytrium dendrobatidis (Bd), which causes the panzootic disease chytridiomycosis. We used 16S rRNA gene metabarcoding to test the adaptive microbiome hypothesis. We compared the community composition, richness, and putative Bd-inhibitory function of the skin microbiome of three amphibian host species in the Pyrenees, as well as three species in Taiwan, in both Bd-positive and negative mountain populations. In both geographical regions, the amphibian host species played a decisive role in shaping the microbial assemblage and putative anti-Bd properties. In the Pyrenees, the species most susceptible to chytridiomycosis, Alytes obstetricans, had the lowest relative abundances of putative protective bacteria. In Bd-positive and negative sites, individuals had different skin microbiomes, with all anuran species showing increased relative abundances of potential anti-Bd bacteria, while the Taiwanese caudata Hynobius sonani showed the opposite pattern. Our results suggest that, in response to exposure to the pathogen, the skin microbiota shifted to a defensive state with increased anti-Bd function, which may contribute to promoting disease resistance, as proposed by the adaptive microbiome hypothesis.
Identifiants
pubmed: 39374928
doi: 10.1111/1462-2920.16699
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e16699Subventions
Organisme : National Council for Scientific and Technological Development - CNPq (Brazil)
Organisme : AXA Research Fund
Organisme : Belmont Forum
ID : ANR-15-MASC-0001-P3
Organisme : Belmont Forum
ID : DFG-SCHM 3059/6-1
Organisme : Belmont Forum
ID : NERC-1633948
Organisme : Belmont Forum
ID : NSF-1633948
Organisme : Belmont Forum
ID : NSFC-41661144004
Informations de copyright
© 2024 The Author(s). Environmental Microbiology published by John Wiley & Sons Ltd.
Références
Anderson, M.J., Walsh, D.C.I. (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecological Monographs, 83(4), 557–574
Bates, K., Sommer, U., Hopkins, K.P., Shelton, J.M.G., Wierzbicki, C., Sergeant, C. et al. (2022) Microbiome function predicts amphibian chytridiomycosis disease dynamics. Microbiome, 10, 44.
Bates, K.A., Clare, F.C., O'Hanlon, S., Bosch, J., Brookes, L., Hopkins, K. et al. (2018) Amphibian chytridiomycosis outbreak dynamics are linked with host skin bacterial community structure. Nature Communications, 9, 693.
Bates, K.A., Shelton, J.M.G., Mercier, V.L., Hopkins, K.P., Harrison, X.A., Petrovan, S.O. et al. (2019) Captivity and infection by the fungal pathogen Batrachochytrium salamandrivorans perturb the amphibian skin microbiome. Frontiers in Microbiology, 10, 1834.
Becker, M.H. & Harris, R.N. (2010) Cutaneous bacteria of the Redback salamander prevent morbidity associated with a lethal disease. PLoS One, 5(6), e10957.
Becker, M.H., Walke, J.B., Cikanek, S., Savage, A.E., Mattheus, N., Santiago, C.N. et al. (2015) Composition of symbiotic bacteria predicts survival in Panamanian Golden frogs infected with a lethal fungus. Proceedings of the Royal Society London B, 282, 20142881.
Becker, M.H., Walke, J.B., Murrill, L., Woodhams, D.C., Reinert, L.K., Rollins‐Smith, L.A. et al. (2015) Phylogenetic distribution of symbiotic bacteria from Panamanian amphibians that inhibit the growth of the lethal fungal pathogen Batrachochytrium dendrobatidis. Molecular Ecology, 24, 1628–1641.
Belden, L.K., Hughey, M.C., Rebollar, E.A., Umile, T.P., Loftus, S.C., Burzynski, E.A. et al. (2015) Panamanian frog species host unique skin bacterial communities. Frontiers in Microbiology, 6, 1171.
Bell, S.C., Alford, R.A., Garland, S., Padilla, G. & Thomas, A.D. (2013) Screening bacterial metabolites for inhibitory effects against Batrachochytrium dendrobatidis using a spectrophotometric assay. Diseases of Aquatic Organisms, 103, 77–85.
Bernardo‐Cravo, A.P., Schmeller, D.S., Chatzinotas, A., Vredenburg, V.T. & Loyau, A. (2020) Environmental factors and host microbiomes shape host‐pathogen dynamics. Trends in Parasitology, 36(7), 616–633.
Bletz, M.C., Loudon, A.H., Becker, M.H., Bell, S.C., Woodhams, D.C., Minbiole, K.P. et al. (2013) Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecology Letters, 16(6), 807–820.
Brucker, R.M., Harris, R.N., Schwantes, C.R., Gallaher, T.N., Flaherty, D.C., Lam, B.A. et al. (2008) Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. Journal of Chemical Ecology, 34, 1422–1429.
Burkart, D., Flechas, S.V., Vredenburg, V.T. & Catenazzi, A. (2017) Cutaneous bacteria, but not peptides, are associated with chytridiomycosis resistance in Peruvian marsupial frogs. Animal Conservation, 20(6), 483–491.
Clare, F.C., Halder, J.B., Daniel, O., Bielby, J., Semenov, M.A., Jombart, T. et al. (2016) Climate forcing of an emerging pathogenic fungus across a montane multi‐host community. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 371(1709), 20150454.
Davis, L.R., Bigler, L. & Woodhams, D.C. (2017) Developmental trajectories of amphibian microbiota: response to bacterial therapy depends on initial community structure. Environmental Microbiology, 19(4), 1502–1517.
Flechas, S.V., Acosta‐González, A., Escobar, L.A., Kueneman, J.G., Sánchez‐Quitian, Z.A., Parra‐Giraldo, C.M. et al. (2019) Microbiota and skin defense peptides may facilitate coexistence of two sympatric Andean frog species with a lethal pathogen. The ISME Journal, 13, 361–373.
Garner, T.W.J., Schmidt, B.R., Martel, A., Pasmans, F., Muths, E., Cunningham, A.A. et al. (2016) Mitigating amphibian chytridiomycoses in nature. Philosophical Transactions of the Royal Society B, 371(1709), 20160207.
Goodwin, K.B., Hutchinson, J.D. & Gompert, Z. (2022) Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd‐inhibitory function in the skin‐associated microbiome of a Rocky Mountain amphibian. Frontiers in Microbiology, 13, 1020329.
Harris, R.N., Brucker, R.M., Walke, J.B., Becker, M.H., Schwantes, C.R., Flaherty, D.C. et al. (2009) Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. The ISME Journal, 3, 818–824.
Harris, R.N., James, T.Y., Lauer, A., Simon, M.A. & Patel, A. (2006) Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth, 3, 53–56.
Harrison, X.A., Price, S.J., Hopkins, K., Leung, W.T.M., Sergeant, C. & Garner, T.W.J. (2019) Diversity‐stability dynamics of the amphibian skin microbiome and susceptibility to a lethal viral pathogen. Frontiers in Microbiology, 10, 2883.
Hollanders, M., Grogan, L.F., Nock, C.J., McCallum, H.I. & Newell, D.A. (2023) Recovered frog populations coexist with endemic Batrachochytrium dendrobatidis despite load‐dependent mortality. Ecological Applications, 33, e2724.
Jani, A.J. & Briggs, C.J. (2014) The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection. Proceedings of the National Academy of Science, 111, E5049–E5058.
Jani, A.J. & Briggs, C.J. (2018) Host and aquatic environment shape the amphibian skin microbiome but effects on downstream resistance to the pathogen Batrachochytrium dendrobatidis are variable. Frontiers in Microbiology, 9, 487.
Jani, A.J., Bushell, J., Arisdakessian, C.G., Belcaid, M., Boiano, D.M., Brown, C. et al. (2021) The amphibian microbiome exhibits poor resilience following pathogen‐induced disturbance. The ISME Journal, 6, 1628–1640.
Jani, A.J., Knapp, R.A. & Briggs, C.J. (2017) Epidemic and endemic pathogen dynamics correspond to distinct host population microbiomes at a landscape scale. Proceedings of the Royal Society B: Biological Sciences, 284, 20170944.
Jiménez, R.R., Carfagno, A., Linhoff, L., Gratwicke, B., Woodhams, D.C., Chafran, L.S. et al. (2022) Inhibitory bacterial diversity and mucosome function differentiate susceptibility of Appalachian salamanders to chytrid fungal infection. Applied and Environmental Microbiology, 88, e0181821.
Jiménez, R.R. & Sommer, S. (2017) The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation. Biodiversity and Conservation, 26, 763–786.
Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S. & Madden, T.L. (2008) NCBI BLAST: a better web interface. Nucleic Acids Research, 36, W5–W9. Available from: https://doi.org/10.1093/nar/gkn201
Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M. et al. (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next‐generation sequencing‐based diversity studies. Nucleic Acids Research, 41(1), e1.
Kruger, A. (2020) Frog skin microbiota vary with host species and environment but not chytrid infection. Frontiers in Microbiology, 11, 1330.
Kueneman, J.G., Wegener Parfrey, L., Woodhams, D.C., Archer, H.M., Knight, R. & McKenzie, V.J. (2014) The amphibian skin‐associated microbiome across species, space and life history stages. Molecular Ecology, 23, 1238–1250.
Kueneman, J.G., Woodhams, D.C., Van Treuren, W., Archer, H.M., Knight, R. & McKenzie, V.J. (2016) Inhibitory bacteria reduce fungi on early life endangered Colorado boreal toads (Anaxyrus boreas). The ISME Journal, 10, 934–944.
Lahtie, L. & Shetty, S. (2012 ‐2019) Microbiome R package. Available from http://microbiome.github.io
Lam, B.A., Walke, J.B., Vredenburg, V.T. & Harris, R.N. (2010) Proportion of individuals with anti‐Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biological Conservation, 143, 529–531.
Longo, A.V., Savage, A.E., Hewson, I. & Zamudio, K.R. (2015) Seasonal and ontogenetic variation of skin microbial communities and relationships to natural disease dynamics in declining amphibians. Royal Society Open Science, 2, 140377.
Loyau, A. (2024) Review of the bacterial Genera known to show anti‐Bd properties. Zenodo. https://doi.org/10.5281/zenodo.11199270
Martínez‐Ugalde, E., Ávila‐Akerberg, V., González Martínez, T.M. & Rebollar, E.A. (2024) Gene functions of the Ambystoma altamirani skin microbiome vary across space and time but potential antifungal genes are widespread and prevalent. Microbial Genomics, 10, 001181.
McMurdie, P.J. & Holmes, S. (2013) An R package for reproductible interactive analysis and graphics of microbiome census data. PLoS One, 8(4), e61217.
Nava‐González, B., Suazo‐Ortuno, I., Bibian Lopez, P., Maldonado‐Lopez, Y., Lopez‐Toledo, L., Raggi, L. et al. (2021) Inhibition of Batrachochytrium dendrobatidis infections by skin bacterial communities in wild amphibian populations. Microbial Ecology, 82, 666–676.
Niederle, M.V., Bosch, J., Ale, C.E., Nader‐Macías, M.E., Aristimuño Ficoseco, C., Toledo, L.F. et al. (2019) Skin‐associated lactic acid bacteria from North American bullfrogs as potential control agents of Batrachochytrium dendrobatidis. PLoS One, 14(9), e0223020.
Oksanen, J., Simpson, G., Blanchet, F., Kindt, R., Legendre, P., Minchin, P. et al. (2022) vegan: community ecology package.
O'Hanlon, S.J., Rieux, A., Farrer, R.A., Rosa, G.M., Waldman, B., Bataille, A. et al. (2018) Recent Asian origin of chytrid fungi causing global amphibian declines. Science, 360, 621–627.
Prest, T.L., Kimball, A.K., Kueneman, J.G. & McKenzie, V.J. (2018) Host‐associated bacterial community succession during amphibian development. Molecular Ecology, 27, 1992–2006.
Rebollar, E.A., Hughey, M.C., Medina, D., Harris, R.N., Ibáñez, R. & Belden, L.K. (2016) Skin bacterial diversity of Panamanian frogs is associated with host susceptibility and presence of Batrachochytrium dendrobatidis. The ISME Journal, 10, 1682–1695.
Rollins‐Smith, L.A. (2009) The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochimica et Biophysica Acta, 1788(8), 1593–1599.
Scheele, B.C., Pasmans, F., Skerratt, L.F., Berger, L., Martel, A., Beukema, W. et al. (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science, 363, 1459–1463.
Schmeller, D.S., Cheng, T., Shelton, J., Lin, C.‐F., Chan‐Alvarado, A., Bernardo‐Cravo, A. et al. (2022) Environment is associated with chytrid infection and skin microbiome richness on an amphibian rich Island (Taiwan). Scientific Reports, 12, 16456.
Siomko, S.A., Greenspan, S.E., Barnett, K.M., Neely, W.J., Chtarbanova, S., Woodhams, D.C. et al. (2023) Selection of anti‐pathogen skin microbiome following prophylaxis treatment in an amphibian model system. Philosophical Transactions of the Royal Society B, 378, 20220126.
Sun, D., Herath, J., Zhou, S., Ellepola, G. & Meegaskumbura, M. (2023) Associations of Batrachochytrium dendrobatidis with skin bacteria and fungi on Asian amphibian hosts. ISME Communications, 3, 123.
Tao, T. Standalone BLAST setup for Unix. 2010 May 31 [Updated 2020 Aug 31]. In: BLAST® Help [Internet]. Bethesda (MD): National Center for Biotechnology Information (US). Available from https://www.ncbi.nlm.nih.gov/books/NBK52640/
Thijs, S., Op De Beeck, M., Beckers, B., Truyens, S., Stevens, V., Van Hamme, J.D. et al. (2017) Comparative evaluation of four bacteria‐specific primer pairs for 16S rRNA gene surveys. Frontiers in Microbiology, 8, 494.
Ujszegi, J., Boroa, Z., Fodor, A., Vajna, B. & Hettyey, A. (2023) Metabolites of Xenorhabdus bacteria are potent candidates for mitigating amphibian chytridiomycosis. AMB Express, 13, 88.
Voyles, J., Woodhams, D.C., Saenz, V., Byrne, A.Q., Perez, R., Rios‐Sotelo, G. et al. (2018) Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation. Science, 359, 1517–1519.
Walke, J.B., Becker, M.H., Hughey, M.C., Swartwout, M.C., Jensen, R.V. & Belden, L.K. (2015) Most of the dominant members of amphibian skin bacteria communities can be readily cultured. Applied and Environmental Microbiology, 81, 6589–6600.
Walke, J.B., Becker, M.H., Loftus, S.C., House, L.L., Cormier, G., Jensen, R.V. et al. (2014) Amphibian skin may select for rare environmental microbes. The ISME Journal, 8, 2207–2217.
Walker, S.F., Bosch, J., Gomez, V., Garner, T.W.J., Cunningham, A.A., Schmeller, D.S. et al. (2010) Factors driving pathogenicity vs. prevalence of amphibian panzootic chytridiomycosis in Iberia. Ecology Letters, 13, 372–382.
Woodhams, D.C., Alford, R.A., Antwis, R.E., Archer, H., Becker, M.H., Belden, L.K. et al. (2015) Antifungal isolates database of amphibian skin‐associated bacteria and function against emerging fungal pathogens. Ecological Archives, E096–E059.
Woodhams, D.C., Bosch, J., Briggs, C.J., Cashins, S., Davis, L.R., Lauer, A. et al. (2011) Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Frontiers in Zoology, 8, 8.
Woodhams, D.C., LaBumbard, B.C., Barnhart, K.L., Becker, M.H., Bletz, M.C., Escobar, L.A. et al. (2018) Prodigiosin, violacein, and volatile organic compounds produced by widespread cutaneous bacteria of amphibians can inhibit two Batrachochytrium fungal pathogens. Microbial Ecology, 75, 1049–1062.
Woodhams, D.C., McCartney, J., Walke, J.B. & Whetstone, R. (2023) The adaptive microbiome hypothesis and immune interactions in amphibian mucus. Developmental and Comparative Immunology, 145, 104690.
Woodhams, D.C., Rollins‐Smith, L.A., Carey, C., Reinert, L., Tyler, M.J. & Alford, R.A. (2006) Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia, 146, 531–540.
Woodhams, D.C., Vredenburg, V.T., Simon, M.A., Billheimer, D., Shakhtour, B., Shyr, Y. et al. (2007) Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow‐legged frog, Rana muscosa. Biological Conservation, 138, 390–398.
Zaneveld, J.R., McMinds, R. & Vega, T.R. (2017) Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nature Microbiology, 2, 1–8.