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Vertebrate Hosts as Islands: Dynamics of Selection, Immigration, Loss, Persistence, and Potential Function of Bacteria on Salamander Skin

Skin bacterial communities can protect amphibians from a fungal pathogen; however, little is known about how these communities are maintained. We used a neutral model of community ecology to identify bacteria that are maintained on salamanders by selection or by dispersal from a bacterial reservoir...

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Autores principales: Loudon, Andrew H., Venkataraman, Arvind, Van Treuren, William, Woodhams, Douglas C., Parfrey, Laura Wegener, McKenzie, Valerie J., Knight, Rob, Schmidt, Thomas M., Harris, Reid N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4793798/
https://www.ncbi.nlm.nih.gov/pubmed/27014249
http://dx.doi.org/10.3389/fmicb.2016.00333
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author Loudon, Andrew H.
Venkataraman, Arvind
Van Treuren, William
Woodhams, Douglas C.
Parfrey, Laura Wegener
McKenzie, Valerie J.
Knight, Rob
Schmidt, Thomas M.
Harris, Reid N.
author_facet Loudon, Andrew H.
Venkataraman, Arvind
Van Treuren, William
Woodhams, Douglas C.
Parfrey, Laura Wegener
McKenzie, Valerie J.
Knight, Rob
Schmidt, Thomas M.
Harris, Reid N.
author_sort Loudon, Andrew H.
collection PubMed
description Skin bacterial communities can protect amphibians from a fungal pathogen; however, little is known about how these communities are maintained. We used a neutral model of community ecology to identify bacteria that are maintained on salamanders by selection or by dispersal from a bacterial reservoir (soil) and ecological drift. We found that 75% (9/12) of bacteria that were consistent with positive selection, <1% of bacteria that were consistent with random dispersal and none of the bacteria that were consistent under negative selection had a 97% or greater match to antifungal isolates. Additionally we performed an experiment where salamanders were either provided or denied a bacterial reservoir and estimated immigration and loss (emigration and local extinction) rates of bacteria on salamanders in both treatments. Loss was strongly related to bacterial richness, suggesting competition is important for structuring the community. Bacteria closely related to antifungal isolates were more likely to persist on salamanders with or without a bacterial reservoir, suggesting they had a competitive advantage. Furthermore, over-represented and under-represented operational taxonomic units (OTUs) had similar persistence on salamanders when a bacterial reservoir was present. However, under-represented OTUs were less likely to persist in the absence of a bacterial reservoir, suggesting that the over-represented and under-represented bacteria were selected against or for on salamanders through time. Our findings from the neutral model, migration and persistence analyses show that bacteria that exhibit a high similarity to antifungal isolates persist on salamanders, which likely protect hosts against pathogens and improve fitness. This research is one of the first to apply ecological theory to investigate assembly of host associated-bacterial communities, which can provide insights for probiotic bioaugmentation as a conservation strategy against disease.
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spelling pubmed-47937982016-03-24 Vertebrate Hosts as Islands: Dynamics of Selection, Immigration, Loss, Persistence, and Potential Function of Bacteria on Salamander Skin Loudon, Andrew H. Venkataraman, Arvind Van Treuren, William Woodhams, Douglas C. Parfrey, Laura Wegener McKenzie, Valerie J. Knight, Rob Schmidt, Thomas M. Harris, Reid N. Front Microbiol Microbiology Skin bacterial communities can protect amphibians from a fungal pathogen; however, little is known about how these communities are maintained. We used a neutral model of community ecology to identify bacteria that are maintained on salamanders by selection or by dispersal from a bacterial reservoir (soil) and ecological drift. We found that 75% (9/12) of bacteria that were consistent with positive selection, <1% of bacteria that were consistent with random dispersal and none of the bacteria that were consistent under negative selection had a 97% or greater match to antifungal isolates. Additionally we performed an experiment where salamanders were either provided or denied a bacterial reservoir and estimated immigration and loss (emigration and local extinction) rates of bacteria on salamanders in both treatments. Loss was strongly related to bacterial richness, suggesting competition is important for structuring the community. Bacteria closely related to antifungal isolates were more likely to persist on salamanders with or without a bacterial reservoir, suggesting they had a competitive advantage. Furthermore, over-represented and under-represented operational taxonomic units (OTUs) had similar persistence on salamanders when a bacterial reservoir was present. However, under-represented OTUs were less likely to persist in the absence of a bacterial reservoir, suggesting that the over-represented and under-represented bacteria were selected against or for on salamanders through time. Our findings from the neutral model, migration and persistence analyses show that bacteria that exhibit a high similarity to antifungal isolates persist on salamanders, which likely protect hosts against pathogens and improve fitness. This research is one of the first to apply ecological theory to investigate assembly of host associated-bacterial communities, which can provide insights for probiotic bioaugmentation as a conservation strategy against disease. Frontiers Media S.A. 2016-03-16 /pmc/articles/PMC4793798/ /pubmed/27014249 http://dx.doi.org/10.3389/fmicb.2016.00333 Text en Copyright © 2016 Loudon, Venkataraman, Van Treuren, Woodhams, Parfrey, McKenzie, Knight, Schmidt and Harris. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Loudon, Andrew H.
Venkataraman, Arvind
Van Treuren, William
Woodhams, Douglas C.
Parfrey, Laura Wegener
McKenzie, Valerie J.
Knight, Rob
Schmidt, Thomas M.
Harris, Reid N.
Vertebrate Hosts as Islands: Dynamics of Selection, Immigration, Loss, Persistence, and Potential Function of Bacteria on Salamander Skin
title Vertebrate Hosts as Islands: Dynamics of Selection, Immigration, Loss, Persistence, and Potential Function of Bacteria on Salamander Skin
title_full Vertebrate Hosts as Islands: Dynamics of Selection, Immigration, Loss, Persistence, and Potential Function of Bacteria on Salamander Skin
title_fullStr Vertebrate Hosts as Islands: Dynamics of Selection, Immigration, Loss, Persistence, and Potential Function of Bacteria on Salamander Skin
title_full_unstemmed Vertebrate Hosts as Islands: Dynamics of Selection, Immigration, Loss, Persistence, and Potential Function of Bacteria on Salamander Skin
title_short Vertebrate Hosts as Islands: Dynamics of Selection, Immigration, Loss, Persistence, and Potential Function of Bacteria on Salamander Skin
title_sort vertebrate hosts as islands: dynamics of selection, immigration, loss, persistence, and potential function of bacteria on salamander skin
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4793798/
https://www.ncbi.nlm.nih.gov/pubmed/27014249
http://dx.doi.org/10.3389/fmicb.2016.00333
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