TY - JOUR
T1 - Identification of intestinal and fecal microbial biomarkers using a porcine social stress model
AU - Nguyen, Tuan Q
AU - Martínez-Álvaro, Marina
AU - Lima, Joana
AU - Auffret, Marc D
AU - Rutherford, Kenneth M D
AU - Simm, Geoff
AU - Dewhurst, Richard J
AU - Baima, Eric T
AU - Roehe, Rainer
N1 - Funding Information:
The research was completed as part of TN’s Ph.D., which was funded by Scotland’s Rural College (SRUC), the Vietnam International Cooperation Department (VICD), the Scottish Government and the University of Edinburgh. The experimental trial and research were funded by the Zoetis Inc. within the Easter Bush Research Consortium (EBRC). The statistical analysis was a collaborative effort supported by funds from the Biotechnology and Biological Sciences Research Council (BBSRC BB/N01720X/1, BB/N016742/1, BB/S006567/1, and BB/S006680/1). All funders were not involved in the study design, collection, analysis, interpretation of data, the writing of this article or the decision to submit it for publication.
Publisher Copyright:
Copyright © 2023 Nguyen, Martínez-Álvaro, Lima, Auffret, Rutherford, Simm, Dewhurst, Baima and Roehe.
PY - 2023/11/9
Y1 - 2023/11/9
N2 - 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.
AB - 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.
KW - porcine microbiota
KW - Stress
KW - growth
KW - feed conversion ratio
KW - feed intake
KW - diversity
KW - pathogen resistance
U2 - 10.3389/fmicb.2023.1197371
DO - 10.3389/fmicb.2023.1197371
M3 - Article
C2 - 38029169
SN - 1664-302X
VL - 14
SP - 1
EP - 16
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
M1 - 1197371
ER -