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Identification of intestinal and fecal microbial biomarkers using a porcine social stress model
Understanding the relationships between social stress and the gastrointestinal microbiota, and how they influence host health and performance is expected to have many scientific and commercial implementations in different species, including identification and improvement of challenges to animal welf...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10670831/ https://www.ncbi.nlm.nih.gov/pubmed/38029169 http://dx.doi.org/10.3389/fmicb.2023.1197371 |
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author | Nguyen, Tuan Q. Martínez-Álvaro, Marina Lima, Joana Auffret, Marc D. Rutherford, Kenneth M. D. Simm, Geoff Dewhurst, Richard J. Baima, Eric T. Roehe, Rainer |
author_facet | Nguyen, Tuan Q. Martínez-Álvaro, Marina Lima, Joana Auffret, Marc D. Rutherford, Kenneth M. D. Simm, Geoff Dewhurst, Richard J. Baima, Eric T. Roehe, Rainer |
author_sort | Nguyen, Tuan Q. |
collection | PubMed |
description | Understanding the relationships between social stress and the gastrointestinal microbiota, and how they influence host health and performance is expected to have many scientific and commercial implementations in different species, including identification and improvement of challenges to animal welfare and health. In particular, the study of the stress impact on the gastrointestinal microbiota of pigs may be of interest as a model for human health. A porcine stress model based on repeated regrouping and reduced space allowance during the last 4 weeks of the finishing period was developed to identify stress-induced changes in the gut microbiome composition. The application of the porcine stress model resulted in a significant increase in salivary cortisol concentration over the course of the trial and decreased growth performance and appetite. The applied social stress resulted in 32 bacteria being either enriched (13) or depleted (19) in the intestine and feces. Fecal samples showed a greater number of microbial genera influenced by stress than caecum or colon samples. Our trial revealed that the opportunistic pathogens Treponema and Clostridium were enriched in colonic and fecal samples from stressed pigs. Additionally, genera such as Streptococcus, Parabacteroides, Desulfovibrio, Terrisporobacter, Marvinbryantia, and Romboutsia were found to be enriched in response to social stress. In contrast, the genera Prevotella, Faecalibacterium, Butyricicoccus, Dialister, Alloprevotella, Megasphaera, and Mitsuokella were depleted. These depleted bacteria are of great interest because they synthesize metabolites [e.g., short-chain fatty acids (SCFA), in particular, butyrate] showing beneficial health benefits due to inhibitory effects on pathogenic bacteria in different animal species. Of particular interest are Dialister and Faecalibacterium, as their depletion was identified in a human study to be associated with inferior quality of life and depression. We also revealed that some pigs were more susceptible to pathogens as indicated by large enrichments of opportunistic pathogens of Clostridium, Treponema, Streptococcus and Campylobacter. Generally, our results provide further evidence for the microbiota-gut-brain axis as indicated by an increase in cortisol concentration due to social stress regulated by the hypothalamic–pituitary–adrenal axis, and a change in microbiota composition, particularly of bacteria known to be associated with pathogenicity and mental health diseases. |
format | Online Article Text |
id | pubmed-10670831 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-106708312023-11-09 Identification of intestinal and fecal microbial biomarkers using a porcine social stress model Nguyen, Tuan Q. Martínez-Álvaro, Marina Lima, Joana Auffret, Marc D. Rutherford, Kenneth M. D. Simm, Geoff Dewhurst, Richard J. Baima, Eric T. Roehe, Rainer Front Microbiol Microbiology Understanding the relationships between social stress and the gastrointestinal microbiota, and how they influence host health and performance is expected to have many scientific and commercial implementations in different species, including identification and improvement of challenges to animal welfare and health. In particular, the study of the stress impact on the gastrointestinal microbiota of pigs may be of interest as a model for human health. A porcine stress model based on repeated regrouping and reduced space allowance during the last 4 weeks of the finishing period was developed to identify stress-induced changes in the gut microbiome composition. The application of the porcine stress model resulted in a significant increase in salivary cortisol concentration over the course of the trial and decreased growth performance and appetite. The applied social stress resulted in 32 bacteria being either enriched (13) or depleted (19) in the intestine and feces. Fecal samples showed a greater number of microbial genera influenced by stress than caecum or colon samples. Our trial revealed that the opportunistic pathogens Treponema and Clostridium were enriched in colonic and fecal samples from stressed pigs. Additionally, genera such as Streptococcus, Parabacteroides, Desulfovibrio, Terrisporobacter, Marvinbryantia, and Romboutsia were found to be enriched in response to social stress. In contrast, the genera Prevotella, Faecalibacterium, Butyricicoccus, Dialister, Alloprevotella, Megasphaera, and Mitsuokella were depleted. These depleted bacteria are of great interest because they synthesize metabolites [e.g., short-chain fatty acids (SCFA), in particular, butyrate] showing beneficial health benefits due to inhibitory effects on pathogenic bacteria in different animal species. Of particular interest are Dialister and Faecalibacterium, as their depletion was identified in a human study to be associated with inferior quality of life and depression. We also revealed that some pigs were more susceptible to pathogens as indicated by large enrichments of opportunistic pathogens of Clostridium, Treponema, Streptococcus and Campylobacter. Generally, our results provide further evidence for the microbiota-gut-brain axis as indicated by an increase in cortisol concentration due to social stress regulated by the hypothalamic–pituitary–adrenal axis, and a change in microbiota composition, particularly of bacteria known to be associated with pathogenicity and mental health diseases. Frontiers Media S.A. 2023-11-09 /pmc/articles/PMC10670831/ /pubmed/38029169 http://dx.doi.org/10.3389/fmicb.2023.1197371 Text en Copyright © 2023 Nguyen, Martínez-Álvaro, Lima, Auffret, Rutherford, Simm, Dewhurst, Baima and Roehe. https://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) and the copyright owner(s) 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 Nguyen, Tuan Q. Martínez-Álvaro, Marina Lima, Joana Auffret, Marc D. Rutherford, Kenneth M. D. Simm, Geoff Dewhurst, Richard J. Baima, Eric T. Roehe, Rainer Identification of intestinal and fecal microbial biomarkers using a porcine social stress model |
title | Identification of intestinal and fecal microbial biomarkers using a porcine social stress model |
title_full | Identification of intestinal and fecal microbial biomarkers using a porcine social stress model |
title_fullStr | Identification of intestinal and fecal microbial biomarkers using a porcine social stress model |
title_full_unstemmed | Identification of intestinal and fecal microbial biomarkers using a porcine social stress model |
title_short | Identification of intestinal and fecal microbial biomarkers using a porcine social stress model |
title_sort | identification of intestinal and fecal microbial biomarkers using a porcine social stress model |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10670831/ https://www.ncbi.nlm.nih.gov/pubmed/38029169 http://dx.doi.org/10.3389/fmicb.2023.1197371 |
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