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

Authors: Ramsay, Timothy; ARFKEN, ANN - Former ARS Employee; Summers, Katie

Submitted to: Animal Microbiome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/28/2022
Publication Date: 11/19/2022
Citation: Ramsay, T.G., Arfken, A.M., Summers, K.L. 2022. Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition.. Animal Microbiome. 4:56. https://doi.org/10.1186/s42523-022-00206-8.
DOI: https://doi.org/10.1186/s42523-022-00206-8

Interpretive Summary: The baby pig undergoes tremendous stress during weaning and this may result in the pig not being able to gain weight. This results in impaired growth and increased risk of infection. Identifying the changes happening in the pig's digestive system during weaning and how those changes communicate with the processes regulating growth in the weanling pig may lead to highly refined probiotics that specifically can target the signals that regulate feed intake and growth to encourage the weanling pig to eat and gain weight. The present study identified a bacteria in the preweaning pig, and only one bacteria of the many thousands in the intestinal tract, that is associated with rapid preweaning growth. This bacteria called Clostridia scindens may have potential to improve piglet performance prior to weaning. Secondly, this study identified several relationships between naturally occurring proteins produced by the intestine and found in the blood, with the intestinal bacteria. These proteins are the communicators between the digestive system and the rest of the body and were shown in this study to be associated with growth during the first 35 days of the young pig's life. Certain bacteria within the intestine were also found to be associated with these specific proteins found in the blood and which may allow development of highly specialized probiotics that target these specific proteins to produce a growth response or help heal a pig having difficulty transitioning from a milk diet to a solid food diet.

Technical Abstract: • Background: Growth rate in the pig 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. ASVs with the greatest correlation with weight gain between day 21-24 belonged to families Prevotellaceae NK3B31 (Spearman's rank correlation coefficient = 0.65, p < 0.001), Veillonellaceae (Spearman's rank correlation coefficient = 0.63, p < 0.001) and Rikenellaceae RC9 (Spearman's rank correlation coefficient = 0.62, p < 0.001). Seven taxa were positively correlated with ADG between day 24-28. Eight taxa were positively correlated with 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 particular ages suggests the potential for developing probiotics that target a specific enteroendocrine response.