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Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino

BACKGROUND: Host microbiomes play a role in hormone production and subsequent fertility in humans, but this is less well understood in non-model organisms. This is of particular relevance to species in zoo-based conservation breeding programmes, as relationships between host microbiome composition a...

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Autores principales: Antwis, Rachael E., Edwards, Katie L., Unwin, Bryony, Walker, Susan L., Shultz, Susanne
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6377766/
https://www.ncbi.nlm.nih.gov/pubmed/30770764
http://dx.doi.org/10.1186/s40168-019-0639-0
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author Antwis, Rachael E.
Edwards, Katie L.
Unwin, Bryony
Walker, Susan L.
Shultz, Susanne
author_facet Antwis, Rachael E.
Edwards, Katie L.
Unwin, Bryony
Walker, Susan L.
Shultz, Susanne
author_sort Antwis, Rachael E.
collection PubMed
description BACKGROUND: Host microbiomes play a role in hormone production and subsequent fertility in humans, but this is less well understood in non-model organisms. This is of particular relevance to species in zoo-based conservation breeding programmes, as relationships between host microbiome composition and reproductive output may allow for the development of microbial augmentation strategies to improve success. Here, we characterise faecal bacterial communities of breeding and non-breeding eastern black rhino (Diceros bicornis michaeli) using 16S rRNA gene amplicon sequencing and quantify progestagen and glucocorticoid metabolite concentrations through enzyme immunoassays to identify such relationships. RESULTS: We identified significant differences in black rhino gut microbiome composition according to ID, institution, breeding success and ovarian cycle phase. In particular, the gut microbiome during pregnancy and post-parturition was significantly altered. Around a third of bacterial genera showed more than ± 10% correlation with either progestagen and/or glucocorticoid concentration, and in general, microbial genera correlated with both hormones in the same direction. Through a combination of analyses, we identified four genera (Aerococcaceae, Atopostipes, Carnobacteriaceae and Solobacterium) that were significantly associated with breeding success, pregnancy and/or post-parturition, and higher faecal progestagen metabolite concentrations. These genera had a lower-than-average relative abundance in the gut microbiome. CONCLUSION: Our results indicate that many members of the gut microbiome of black rhino are associated with hormone production and breeding success, and some members of the rare microbiota appear to be particularly important. Although the directionality of the relationship is unclear, the variation in gut microbiome communities represents a potential biomarker of reproductive health. We identified four genera that were associated with multiple indicators of reproductive output; these could be candidate probiotics to improve the breeding success of black rhino in zoo-based conservation breeding programmes. Further work is required to understand the efficacy and feasibility of this, either directly through microbial augmentation (e.g. probiotics) or indirectly via dietary manipulation or prebiotics. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0639-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-63777662019-02-27 Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino Antwis, Rachael E. Edwards, Katie L. Unwin, Bryony Walker, Susan L. Shultz, Susanne Microbiome Research BACKGROUND: Host microbiomes play a role in hormone production and subsequent fertility in humans, but this is less well understood in non-model organisms. This is of particular relevance to species in zoo-based conservation breeding programmes, as relationships between host microbiome composition and reproductive output may allow for the development of microbial augmentation strategies to improve success. Here, we characterise faecal bacterial communities of breeding and non-breeding eastern black rhino (Diceros bicornis michaeli) using 16S rRNA gene amplicon sequencing and quantify progestagen and glucocorticoid metabolite concentrations through enzyme immunoassays to identify such relationships. RESULTS: We identified significant differences in black rhino gut microbiome composition according to ID, institution, breeding success and ovarian cycle phase. In particular, the gut microbiome during pregnancy and post-parturition was significantly altered. Around a third of bacterial genera showed more than ± 10% correlation with either progestagen and/or glucocorticoid concentration, and in general, microbial genera correlated with both hormones in the same direction. Through a combination of analyses, we identified four genera (Aerococcaceae, Atopostipes, Carnobacteriaceae and Solobacterium) that were significantly associated with breeding success, pregnancy and/or post-parturition, and higher faecal progestagen metabolite concentrations. These genera had a lower-than-average relative abundance in the gut microbiome. CONCLUSION: Our results indicate that many members of the gut microbiome of black rhino are associated with hormone production and breeding success, and some members of the rare microbiota appear to be particularly important. Although the directionality of the relationship is unclear, the variation in gut microbiome communities represents a potential biomarker of reproductive health. We identified four genera that were associated with multiple indicators of reproductive output; these could be candidate probiotics to improve the breeding success of black rhino in zoo-based conservation breeding programmes. Further work is required to understand the efficacy and feasibility of this, either directly through microbial augmentation (e.g. probiotics) or indirectly via dietary manipulation or prebiotics. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0639-0) contains supplementary material, which is available to authorized users. BioMed Central 2019-02-15 /pmc/articles/PMC6377766/ /pubmed/30770764 http://dx.doi.org/10.1186/s40168-019-0639-0 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Antwis, Rachael E.
Edwards, Katie L.
Unwin, Bryony
Walker, Susan L.
Shultz, Susanne
Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino
title Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino
title_full Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino
title_fullStr Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino
title_full_unstemmed Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino
title_short Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino
title_sort rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6377766/
https://www.ncbi.nlm.nih.gov/pubmed/30770764
http://dx.doi.org/10.1186/s40168-019-0639-0
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