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Metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction

Newborn animals with intrauterine growth restriction (IUGR) are characterized by impaired intestinal structure and function; however, their intestinal microbiota and metabolome profiles have not been fully identified. The present study investigated the differences in colonic microbiota, metabolomics...

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Autores principales: Tang, Wu, Zhang, Wanghong, Azad, Md. Abul Kalam, Ma, Cui, Zhu, Qian, Kong, Xiangfeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9518826/
https://www.ncbi.nlm.nih.gov/pubmed/36187985
http://dx.doi.org/10.3389/fmicb.2022.989060
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author Tang, Wu
Zhang, Wanghong
Azad, Md. Abul Kalam
Ma, Cui
Zhu, Qian
Kong, Xiangfeng
author_facet Tang, Wu
Zhang, Wanghong
Azad, Md. Abul Kalam
Ma, Cui
Zhu, Qian
Kong, Xiangfeng
author_sort Tang, Wu
collection PubMed
description Newborn animals with intrauterine growth restriction (IUGR) are characterized by impaired intestinal structure and function; however, their intestinal microbiota and metabolome profiles have not been fully identified. The present study investigated the differences in colonic microbiota, metabolomics, and barrier function-related gene expression profiles between the IUGR and normal birth weight (NBW) piglets at 7, 21, and 28 days of age. Forty-eight piglets (24 NBW and 24 IUGR) from 24 litters were assigned to assess the differences in colonic microbiota, metabolomics, and gene expression between IUGR and NBW piglets. Compared with the NBW piglets, IUGR piglets showed decreased Shannon index and increased Simpson index at 7 days of age and Chao1 index at 21 days of age (p < 0.05). The IUGR piglets had lower abundances of Firmicutes, Subdoligranulum, Ruminococcaceae_UCG-002, and Ruminococcaceae_UCG-003 at 7 days of age, and Bacteroidetes, Phascolarctobacterium, and Ruminococcaceae_UCG-005 at 21 days of age, when compared with the NBW piglets (p < 0.05). Metabolomics analysis showed significant changes in 147 metabolites mainly involved in organic acids and their derivatives in the colon. Six differential metabolic pathways were significantly enriched, including purine metabolism, amino sugar/nucleotide sugar metabolism, ubiquinone/other terpenoid-quinone biosynthesis, phenylalanine/tyrosine/tryptophan biosynthesis, phenylalanine metabolism, and histidine metabolism. Spearman’s correlation analysis further demonstrated significant correlations between colonic microbiota and metabolites. In addition, colonic isobutyrate at 7 days of age, isovalerate and total short-chain fatty acids (SCFAs) at 21 days of age, and acetate, propionate, butyrate, and total SCFAs levels at 28 days of age were lower and isovalerate was higher at 28 days of age in the IUGR piglets than in the NBW piglets (p < 0.05). Furthermore, the mRNA expression of zonula occludens (ZO)-1 at 7 days of age, ZO-1, occludin, and interleukin (IL)-4 at 21 days of age were down-regulated in the IUGR piglets, whereas tumor necrosis factor (TNF)-α and nuclear factor-kappa B (NF-κB) at 28 days of age were up-regulated, when compared with the NBW piglets (p < 0.05). The findings suggest that the IUGR pigs present abnormal microbiota and nutrient metabolism in the colon, which may further affect the intestine barrier function by regulating gene expressions.
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spelling pubmed-95188262022-09-29 Metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction Tang, Wu Zhang, Wanghong Azad, Md. Abul Kalam Ma, Cui Zhu, Qian Kong, Xiangfeng Front Microbiol Microbiology Newborn animals with intrauterine growth restriction (IUGR) are characterized by impaired intestinal structure and function; however, their intestinal microbiota and metabolome profiles have not been fully identified. The present study investigated the differences in colonic microbiota, metabolomics, and barrier function-related gene expression profiles between the IUGR and normal birth weight (NBW) piglets at 7, 21, and 28 days of age. Forty-eight piglets (24 NBW and 24 IUGR) from 24 litters were assigned to assess the differences in colonic microbiota, metabolomics, and gene expression between IUGR and NBW piglets. Compared with the NBW piglets, IUGR piglets showed decreased Shannon index and increased Simpson index at 7 days of age and Chao1 index at 21 days of age (p < 0.05). The IUGR piglets had lower abundances of Firmicutes, Subdoligranulum, Ruminococcaceae_UCG-002, and Ruminococcaceae_UCG-003 at 7 days of age, and Bacteroidetes, Phascolarctobacterium, and Ruminococcaceae_UCG-005 at 21 days of age, when compared with the NBW piglets (p < 0.05). Metabolomics analysis showed significant changes in 147 metabolites mainly involved in organic acids and their derivatives in the colon. Six differential metabolic pathways were significantly enriched, including purine metabolism, amino sugar/nucleotide sugar metabolism, ubiquinone/other terpenoid-quinone biosynthesis, phenylalanine/tyrosine/tryptophan biosynthesis, phenylalanine metabolism, and histidine metabolism. Spearman’s correlation analysis further demonstrated significant correlations between colonic microbiota and metabolites. In addition, colonic isobutyrate at 7 days of age, isovalerate and total short-chain fatty acids (SCFAs) at 21 days of age, and acetate, propionate, butyrate, and total SCFAs levels at 28 days of age were lower and isovalerate was higher at 28 days of age in the IUGR piglets than in the NBW piglets (p < 0.05). Furthermore, the mRNA expression of zonula occludens (ZO)-1 at 7 days of age, ZO-1, occludin, and interleukin (IL)-4 at 21 days of age were down-regulated in the IUGR piglets, whereas tumor necrosis factor (TNF)-α and nuclear factor-kappa B (NF-κB) at 28 days of age were up-regulated, when compared with the NBW piglets (p < 0.05). The findings suggest that the IUGR pigs present abnormal microbiota and nutrient metabolism in the colon, which may further affect the intestine barrier function by regulating gene expressions. Frontiers Media S.A. 2022-09-14 /pmc/articles/PMC9518826/ /pubmed/36187985 http://dx.doi.org/10.3389/fmicb.2022.989060 Text en Copyright © 2022 Tang, Zhang, Azad, Ma, Zhu and Kong. 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
Tang, Wu
Zhang, Wanghong
Azad, Md. Abul Kalam
Ma, Cui
Zhu, Qian
Kong, Xiangfeng
Metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction
title Metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction
title_full Metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction
title_fullStr Metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction
title_full_unstemmed Metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction
title_short Metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction
title_sort metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9518826/
https://www.ncbi.nlm.nih.gov/pubmed/36187985
http://dx.doi.org/10.3389/fmicb.2022.989060
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