Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibian
Host-associated microbiomes play important roles in host health and pathogen defense. In amphibians, the skin-associated microbiota can contribute to innate immunity with potential implications for disease management. Few studies have examined season-long temporal variation in the amphibian skin-ass...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-12-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1020329/full |
| _version_ | 1811178250166075392 |
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| author | Kenen B. Goodwin Kenen B. Goodwin Jaren D. Hutchinson Zachariah Gompert |
| author_facet | Kenen B. Goodwin Kenen B. Goodwin Jaren D. Hutchinson Zachariah Gompert |
| author_sort | Kenen B. Goodwin |
| collection | DOAJ |
| description | Host-associated microbiomes play important roles in host health and pathogen defense. In amphibians, the skin-associated microbiota can contribute to innate immunity with potential implications for disease management. Few studies have examined season-long temporal variation in the amphibian skin-associated microbiome, and the interactions between bacteria and fungi on amphibian skin remain poorly understood. We characterize season-long temporal variation in the skin-associated microbiome of the western tiger salamander (Ambystoma mavortium) for both bacteria and fungi between sites and across salamander life stages. Two hundred seven skin-associated microbiome samples were collected from salamanders at two Rocky Mountain lakes throughout the summer and fall of 2018, and 127 additional microbiome samples were collected from lake water and lake substrate. We used 16S rRNA and ITS amplicon sequencing with Bayesian Dirichlet-multinomial regression to estimate the relative abundances of bacterial and fungal taxa, test for differential abundance, examine microbial selection, and derive alpha diversity. We predicted the ability of bacterial communities to inhibit the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd), a cutaneous fungal pathogen, using stochastic character mapping and a database of Bd-inhibitory bacterial isolates. For both bacteria and fungi, we observed variation in community composition through time, between sites, and with salamander age and life stage. We further found that temporal trends in community composition were specific to each combination of salamander age, life stage, and lake. We found salamander skin to be selective for microbes, with many taxa disproportionately represented relative to the environment. Salamander skin appeared to select for predicted Bd-inhibitory bacteria, and we found a negative relationship between the relative abundances of predicted Bd-inhibitory bacteria and Bd. We hope these findings will assist in the conservation of amphibian species threatened by chytridiomycosis and other emerging diseases. |
| first_indexed | 2024-04-11T06:16:33Z |
| format | Article |
| id | doaj.art-740d7e73005e4cceae07845a9cd4c19e |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-11T06:16:33Z |
| publishDate | 2022-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-740d7e73005e4cceae07845a9cd4c19e2022-12-22T04:41:03ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-12-011310.3389/fmicb.2022.10203291020329Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibianKenen B. Goodwin0Kenen B. Goodwin1Jaren D. Hutchinson2Zachariah Gompert3Department of Watershed Sciences, Utah State University, Logan, UT, United StatesDepartment of Wildland Resources, Utah State University, Logan, UT, United StatesDepartment of Wildland Resources, Utah State University, Logan, UT, United StatesDepartment of Biology, Utah State University, Logan, UT, United StatesHost-associated microbiomes play important roles in host health and pathogen defense. In amphibians, the skin-associated microbiota can contribute to innate immunity with potential implications for disease management. Few studies have examined season-long temporal variation in the amphibian skin-associated microbiome, and the interactions between bacteria and fungi on amphibian skin remain poorly understood. We characterize season-long temporal variation in the skin-associated microbiome of the western tiger salamander (Ambystoma mavortium) for both bacteria and fungi between sites and across salamander life stages. Two hundred seven skin-associated microbiome samples were collected from salamanders at two Rocky Mountain lakes throughout the summer and fall of 2018, and 127 additional microbiome samples were collected from lake water and lake substrate. We used 16S rRNA and ITS amplicon sequencing with Bayesian Dirichlet-multinomial regression to estimate the relative abundances of bacterial and fungal taxa, test for differential abundance, examine microbial selection, and derive alpha diversity. We predicted the ability of bacterial communities to inhibit the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd), a cutaneous fungal pathogen, using stochastic character mapping and a database of Bd-inhibitory bacterial isolates. For both bacteria and fungi, we observed variation in community composition through time, between sites, and with salamander age and life stage. We further found that temporal trends in community composition were specific to each combination of salamander age, life stage, and lake. We found salamander skin to be selective for microbes, with many taxa disproportionately represented relative to the environment. Salamander skin appeared to select for predicted Bd-inhibitory bacteria, and we found a negative relationship between the relative abundances of predicted Bd-inhibitory bacteria and Bd. We hope these findings will assist in the conservation of amphibian species threatened by chytridiomycosis and other emerging diseases.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1020329/fulltemporal variationspatial variationbacteriafungirelative abundanceBayesian analysis |
| spellingShingle | Kenen B. Goodwin Kenen B. Goodwin Jaren D. Hutchinson Zachariah Gompert Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibian Frontiers in Microbiology temporal variation spatial variation bacteria fungi relative abundance Bayesian analysis |
| title | Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibian |
| title_full | Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibian |
| title_fullStr | Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibian |
| title_full_unstemmed | Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibian |
| title_short | Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibian |
| title_sort | spatiotemporal and ontogenetic variation microbial selection and predicted bd inhibitory function in the skin associated microbiome of a rocky mountain amphibian |
| topic | temporal variation spatial variation bacteria fungi relative abundance Bayesian analysis |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1020329/full |
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