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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
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.
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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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