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Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota

Infection by gastrointestinal helminths of humans, livestock and wild animals is common, but the impact of such endoparasites on wild hosts and their gut microbiota represents an important overlooked component of population dynamics. Wild host gut microbiota and endoparasites occupy the same physica...

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Autores principales: Newbold, Lindsay K, Burthe, Sarah J, Oliver, Anna E, Gweon, Hyun S, Barnes, Christopher J, Daunt, Francis, van der Gast, Christopher J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322305/
https://www.ncbi.nlm.nih.gov/pubmed/27983724
http://dx.doi.org/10.1038/ismej.2016.153
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author Newbold, Lindsay K
Burthe, Sarah J
Oliver, Anna E
Gweon, Hyun S
Barnes, Christopher J
Daunt, Francis
van der Gast, Christopher J
author_facet Newbold, Lindsay K
Burthe, Sarah J
Oliver, Anna E
Gweon, Hyun S
Barnes, Christopher J
Daunt, Francis
van der Gast, Christopher J
author_sort Newbold, Lindsay K
collection PubMed
description Infection by gastrointestinal helminths of humans, livestock and wild animals is common, but the impact of such endoparasites on wild hosts and their gut microbiota represents an important overlooked component of population dynamics. Wild host gut microbiota and endoparasites occupy the same physical niche spaces with both affecting host nutrition and health. However, associations between the two are poorly understood. Here we used the commonly parasitized European shag (Phalacrocorax aristotelis) as a model wild host. Forty live adults from the same colony were sampled. Endoscopy was employed to quantify helminth infection in situ. Microbiota from the significantly distinct proventriculus (site of infection), cloacal and faecal gastrointestinal tract microbiomes were characterised using 16S rRNA gene-targeted high-throughput sequencing. We found increasingly strong associations between helminth infection and microbiota composition progressing away from the site of infection, observing a pronounced dysbiosis in microbiota when samples were partitioned into high- and low-burden groups. We posit this dysbiosis is predominately explained by helminths inducing an anti-inflammatory environment in the proventriculus, diverting host immune responses away from themselves. This study, within live wild animals, provides a vital foundation to better understand the mechanisms that underpin the three-way relationship between helminths, microbiota and hosts.
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spelling pubmed-53223052017-03-01 Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota Newbold, Lindsay K Burthe, Sarah J Oliver, Anna E Gweon, Hyun S Barnes, Christopher J Daunt, Francis van der Gast, Christopher J ISME J Original Article Infection by gastrointestinal helminths of humans, livestock and wild animals is common, but the impact of such endoparasites on wild hosts and their gut microbiota represents an important overlooked component of population dynamics. Wild host gut microbiota and endoparasites occupy the same physical niche spaces with both affecting host nutrition and health. However, associations between the two are poorly understood. Here we used the commonly parasitized European shag (Phalacrocorax aristotelis) as a model wild host. Forty live adults from the same colony were sampled. Endoscopy was employed to quantify helminth infection in situ. Microbiota from the significantly distinct proventriculus (site of infection), cloacal and faecal gastrointestinal tract microbiomes were characterised using 16S rRNA gene-targeted high-throughput sequencing. We found increasingly strong associations between helminth infection and microbiota composition progressing away from the site of infection, observing a pronounced dysbiosis in microbiota when samples were partitioned into high- and low-burden groups. We posit this dysbiosis is predominately explained by helminths inducing an anti-inflammatory environment in the proventriculus, diverting host immune responses away from themselves. This study, within live wild animals, provides a vital foundation to better understand the mechanisms that underpin the three-way relationship between helminths, microbiota and hosts. Nature Publishing Group 2017-03 2016-12-16 /pmc/articles/PMC5322305/ /pubmed/27983724 http://dx.doi.org/10.1038/ismej.2016.153 Text en Copyright © 2017 International Society for Microbial Ecology http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Original Article
Newbold, Lindsay K
Burthe, Sarah J
Oliver, Anna E
Gweon, Hyun S
Barnes, Christopher J
Daunt, Francis
van der Gast, Christopher J
Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota
title Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota
title_full Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota
title_fullStr Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota
title_full_unstemmed Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota
title_short Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota
title_sort helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322305/
https://www.ncbi.nlm.nih.gov/pubmed/27983724
http://dx.doi.org/10.1038/ismej.2016.153
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