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Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition

BACKGROUND: Growth rate in pigs can be affected by numerous factors that also affect feeding behavior and the microbiome. Recent studies report some communication between the microbiome and the enteroendocrine system. The present study examined if changes in the piglet microbiome between birth and d...

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Autores principales: Ramsay, T. G., Arfken, A. M., Summers, K. L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9673406/
https://www.ncbi.nlm.nih.gov/pubmed/36401290
http://dx.doi.org/10.1186/s42523-022-00206-8
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author Ramsay, T. G.
Arfken, A. M.
Summers, K. L.
author_facet Ramsay, T. G.
Arfken, A. M.
Summers, K. L.
author_sort Ramsay, T. G.
collection PubMed
description BACKGROUND: Growth rate in pigs can be affected by numerous factors that also affect feeding behavior and the microbiome. Recent studies report some communication between the microbiome and the enteroendocrine system. The present study examined if changes in the piglet microbiome between birth and during the weaning transition can be correlated either positively or negatively with growth rate and plasma concentrations of enteroendocrine peptides. RESULTS: During the post-weaning transition, a 49% reduction in average daily gain was observed at day 24 (P < 0.05) relative to day 21. Pigs recovered by day 28 with body weight and average daily gain increases of 17% and 175%, respectively relative to day 24 and the highest rate of gain was measured at day 35 (462 g/day). The time interval between day 21–24 had the highest number of correlations (n = 25) between the relative abundance differences in taxa over time and corresponding percent weight gain. Amplicon sequence variants with the greatest correlation with percent weight gain between day 21–24 belonged to families Prevotellaceae NK3B31 (ρ = 0.65, P < 0.001), Veillonellaceae (ρ = 0.63, P < 0.001) and Rikenellaceae RC9 (ρ = 0.62, P < 0.001). Seven taxa were positively correlated with percent weight gain between day 24–28. Eight taxa were positively correlated with percent weight gain between day 28–35, of which four were Clostridia. Only Lactobacillus reuteri was positively correlated across both day 24–28 and day 28–35 analyses. Insulin-like growth factor 1 (IGF-1; R2 = 0.61, P < 0.001), glucose-dependent insulinotropic polypeptide (GIP; R2 = 0.20, P < 0.001), glucagon-like peptide 1 (GLP-1; R2 = 0.51, P < 0.001), and glucagon-like peptide 2 (GLP-2; R2 = 0.21, P < 0.001) were significantly associated with the piglet fecal community NMDS, while serotonin showed no significant association (R2 = 0.03, P = 0.15). Higher concentrations of GLP-1 and GLP-2 characterized day 1 fecal communities, while GIP levels had the strongest relationship primarily with samples ordinated with the day 21 cluster. CONCLUSIONS: Demonstration of an association of certain taxa with individual gut peptides at specific ages suggests the potential for the microbiome to elicit changes in the gut enteroendocrine system during early postnatal development in the pig. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00206-8.
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spelling pubmed-96734062022-11-19 Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition Ramsay, T. G. Arfken, A. M. Summers, K. L. Anim Microbiome Research Article BACKGROUND: Growth rate in pigs can be affected by numerous factors that also affect feeding behavior and the microbiome. Recent studies report some communication between the microbiome and the enteroendocrine system. The present study examined if changes in the piglet microbiome between birth and during the weaning transition can be correlated either positively or negatively with growth rate and plasma concentrations of enteroendocrine peptides. RESULTS: During the post-weaning transition, a 49% reduction in average daily gain was observed at day 24 (P < 0.05) relative to day 21. Pigs recovered by day 28 with body weight and average daily gain increases of 17% and 175%, respectively relative to day 24 and the highest rate of gain was measured at day 35 (462 g/day). The time interval between day 21–24 had the highest number of correlations (n = 25) between the relative abundance differences in taxa over time and corresponding percent weight gain. Amplicon sequence variants with the greatest correlation with percent weight gain between day 21–24 belonged to families Prevotellaceae NK3B31 (ρ = 0.65, P < 0.001), Veillonellaceae (ρ = 0.63, P < 0.001) and Rikenellaceae RC9 (ρ = 0.62, P < 0.001). Seven taxa were positively correlated with percent weight gain between day 24–28. Eight taxa were positively correlated with percent weight gain between day 28–35, of which four were Clostridia. Only Lactobacillus reuteri was positively correlated across both day 24–28 and day 28–35 analyses. Insulin-like growth factor 1 (IGF-1; R2 = 0.61, P < 0.001), glucose-dependent insulinotropic polypeptide (GIP; R2 = 0.20, P < 0.001), glucagon-like peptide 1 (GLP-1; R2 = 0.51, P < 0.001), and glucagon-like peptide 2 (GLP-2; R2 = 0.21, P < 0.001) were significantly associated with the piglet fecal community NMDS, while serotonin showed no significant association (R2 = 0.03, P = 0.15). Higher concentrations of GLP-1 and GLP-2 characterized day 1 fecal communities, while GIP levels had the strongest relationship primarily with samples ordinated with the day 21 cluster. CONCLUSIONS: Demonstration of an association of certain taxa with individual gut peptides at specific ages suggests the potential for the microbiome to elicit changes in the gut enteroendocrine system during early postnatal development in the pig. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00206-8. BioMed Central 2022-11-18 /pmc/articles/PMC9673406/ /pubmed/36401290 http://dx.doi.org/10.1186/s42523-022-00206-8 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/) .
spellingShingle Research Article
Ramsay, T. G.
Arfken, A. M.
Summers, K. L.
Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition
title Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition
title_full Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition
title_fullStr Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition
title_full_unstemmed Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition
title_short Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition
title_sort enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9673406/
https://www.ncbi.nlm.nih.gov/pubmed/36401290
http://dx.doi.org/10.1186/s42523-022-00206-8
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