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Environmental and maternal factors shaping tonsillar microbiota development in piglets

BACKGROUND: The palatine tonsils are part of the mucosal immune system and stimulate immune responses through M cell uptake sampling of antigens and bacteria in the tonsillar crypts. Little is known about the development of the tonsillar microbiota and the factors determining the establishment and p...

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Autores principales: Fredriksen, Simen, Guan, Xiaonan, Boekhorst, Jos, Molist, Francesc, van Baarlen, Peter, Wells, Jerry M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9513891/
https://www.ncbi.nlm.nih.gov/pubmed/36163011
http://dx.doi.org/10.1186/s12866-022-02625-8
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author Fredriksen, Simen
Guan, Xiaonan
Boekhorst, Jos
Molist, Francesc
van Baarlen, Peter
Wells, Jerry M.
author_facet Fredriksen, Simen
Guan, Xiaonan
Boekhorst, Jos
Molist, Francesc
van Baarlen, Peter
Wells, Jerry M.
author_sort Fredriksen, Simen
collection PubMed
description BACKGROUND: The palatine tonsils are part of the mucosal immune system and stimulate immune responses through M cell uptake sampling of antigens and bacteria in the tonsillar crypts. Little is known about the development of the tonsillar microbiota and the factors determining the establishment and proliferation of disease-associated bacteria such as Streptococcus suis. In this study, we assessed tonsillar microbiota development in piglets during the first 5 weeks of life and identified the relative importance of maternal and environmental farm parameters influencing the tonsillar microbiota at different ages. Additionally, we studied the effect sow vaccination with a bacterin against S. suis on microbiota development and S. suis colonisation in their offspring. RESULTS: Amplicon sequencing of the 16S rRNA gene V3-V4 region revealed that a diverse tonsillar microbiota is established shortly after birth, which then gradually changes during the first 5 weeks of life without a large impact of weaning on composition or diversity. We found a strong litter effect, with siblings sharing a more similar microbiota compared to non-sibling piglets. Co-housing in rooms, within which litters were housed in separate pens, also had a large impact on microbiota composition. Sow parity and prepartum S. suis bacterin vaccination of sows had weaker but significant associations with microbiota composition, impacting on the abundance of Streptococcus species before and after weaning. Sex and birthweight had limited impact on the tonsillar microbiota, and none of the measured factors had consistent associations with microbiota diversity. CONCLUSIONS: The piglet tonsillar microbiota is established shortly after birth. While microbiota development is associated with both environmental and maternal parameters, weaning has limited impact on microbiota composition. Intramuscular vaccination of sows pre-partum had a significant effect on the tonsillar microbiota composition of their piglets. These findings provide new insights into the mechanisms shaping the tonsillar microbiota. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-022-02625-8.
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spelling pubmed-95138912022-09-28 Environmental and maternal factors shaping tonsillar microbiota development in piglets Fredriksen, Simen Guan, Xiaonan Boekhorst, Jos Molist, Francesc van Baarlen, Peter Wells, Jerry M. BMC Microbiol Research BACKGROUND: The palatine tonsils are part of the mucosal immune system and stimulate immune responses through M cell uptake sampling of antigens and bacteria in the tonsillar crypts. Little is known about the development of the tonsillar microbiota and the factors determining the establishment and proliferation of disease-associated bacteria such as Streptococcus suis. In this study, we assessed tonsillar microbiota development in piglets during the first 5 weeks of life and identified the relative importance of maternal and environmental farm parameters influencing the tonsillar microbiota at different ages. Additionally, we studied the effect sow vaccination with a bacterin against S. suis on microbiota development and S. suis colonisation in their offspring. RESULTS: Amplicon sequencing of the 16S rRNA gene V3-V4 region revealed that a diverse tonsillar microbiota is established shortly after birth, which then gradually changes during the first 5 weeks of life without a large impact of weaning on composition or diversity. We found a strong litter effect, with siblings sharing a more similar microbiota compared to non-sibling piglets. Co-housing in rooms, within which litters were housed in separate pens, also had a large impact on microbiota composition. Sow parity and prepartum S. suis bacterin vaccination of sows had weaker but significant associations with microbiota composition, impacting on the abundance of Streptococcus species before and after weaning. Sex and birthweight had limited impact on the tonsillar microbiota, and none of the measured factors had consistent associations with microbiota diversity. CONCLUSIONS: The piglet tonsillar microbiota is established shortly after birth. While microbiota development is associated with both environmental and maternal parameters, weaning has limited impact on microbiota composition. Intramuscular vaccination of sows pre-partum had a significant effect on the tonsillar microbiota composition of their piglets. These findings provide new insights into the mechanisms shaping the tonsillar microbiota. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-022-02625-8. BioMed Central 2022-09-26 /pmc/articles/PMC9513891/ /pubmed/36163011 http://dx.doi.org/10.1186/s12866-022-02625-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Fredriksen, Simen
Guan, Xiaonan
Boekhorst, Jos
Molist, Francesc
van Baarlen, Peter
Wells, Jerry M.
Environmental and maternal factors shaping tonsillar microbiota development in piglets
title Environmental and maternal factors shaping tonsillar microbiota development in piglets
title_full Environmental and maternal factors shaping tonsillar microbiota development in piglets
title_fullStr Environmental and maternal factors shaping tonsillar microbiota development in piglets
title_full_unstemmed Environmental and maternal factors shaping tonsillar microbiota development in piglets
title_short Environmental and maternal factors shaping tonsillar microbiota development in piglets
title_sort environmental and maternal factors shaping tonsillar microbiota development in piglets
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9513891/
https://www.ncbi.nlm.nih.gov/pubmed/36163011
http://dx.doi.org/10.1186/s12866-022-02625-8
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