Undernutrition disrupts jejunal and ileal microbiota and epithelial tissue homeostasis in a pregnant sheep model

Nutrition consistently affects microbe-host interactions in the gastrointestinal tract. This study aimed to unravel how undernutrition reshapes the microbial composition and the homeostasis of epithelium in the jejunum and ileum. Sixteen late-gestation Hu-sheep were randomly assigned to the control...

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Main Authors: Weibin Wu, Muhammad Faheem Akhtar, Jiahong Geng, Huizhen Lu, Muhammad Ajwad Rahim, Jianbo Cheng, Xiaoling Ding, Shengyong Mao, Yanfeng Xue
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2025-03-01
Series:Animal Nutrition
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Online Access:http://www.sciencedirect.com/science/article/pii/S2405654524001513
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author Weibin Wu
Muhammad Faheem Akhtar
Jiahong Geng
Huizhen Lu
Muhammad Ajwad Rahim
Jianbo Cheng
Xiaoling Ding
Shengyong Mao
Yanfeng Xue
author_facet Weibin Wu
Muhammad Faheem Akhtar
Jiahong Geng
Huizhen Lu
Muhammad Ajwad Rahim
Jianbo Cheng
Xiaoling Ding
Shengyong Mao
Yanfeng Xue
author_sort Weibin Wu
collection DOAJ
description Nutrition consistently affects microbe-host interactions in the gastrointestinal tract. This study aimed to unravel how undernutrition reshapes the microbial composition and the homeostasis of epithelium in the jejunum and ileum. Sixteen late-gestation Hu-sheep were randomly assigned to the control group (n = 8, 100% ad libitum feeding levels) or the undernutrition group (n = 8, which received 30% ad libitum feeding levels). After 15-d treatment, all ewes were slaughtered, and jejunal and ileal digesta and epithelium samples were collected for 16S rRNA gene sequencing and transcriptome sequencing, respectively. Results indicated that undernutrition decreased the jejunal and ileal tissue weights (P = 0.005 and P = 0.022) and the levels of volatile fatty acids (P = 0.019 and P = 0.007) and microbial protein levels (P = 0.019 and P = 0.031) in jejunal and ileal digesta. The relative abundance of acetate producing microbiota, including Clostridia UCG-014 norank, Ruminococcus, [Ruminococcus] gauvreauii, and Lachnospiraceae_Blautia, were significantly reduced (P < 0.05) in the jejunum and ileum. Undernutrition up-regulated (P < 0.05) the expression of genes involved in amino acid synthesis and fatty acid oxidation, but down-regulated (P < 0.05) the expression of genes associated with amino acid degradation, fatty acid synthesis, and extracellular structures in jejunal and ileal epithelium. In the jejunal epithelium, genes associated with extracellular matrix–receptor interactions, cell growth, and immune response were down-regulated (P < 0.05) upon undernutrition. Taken together, undernutrition changed the microbial community in the jejunum and ileum, which altered the fermentation mode and the production of volatile fatty acids and microbial protein. These affected the energy and protein system in the epithelium and reprogrammed substance metabolism and extracellular structures, which probably further influenced cell growth and immune response. These insights provide a foundation for completely clarifying the crosstalk between small intestinal microbiota and the host.
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publisher KeAi Communications Co., Ltd.
record_format Article
series Animal Nutrition
spelling doaj-art-6f3bcbd6cc37447ab53af94fad9d40352025-02-07T04:47:52ZengKeAi Communications Co., Ltd.Animal Nutrition2405-65452025-03-0120263276Undernutrition disrupts jejunal and ileal microbiota and epithelial tissue homeostasis in a pregnant sheep modelWeibin Wu0Muhammad Faheem Akhtar1Jiahong Geng2Huizhen Lu3Muhammad Ajwad Rahim4Jianbo Cheng5Xiaoling Ding6Shengyong Mao7Yanfeng Xue8College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, Anhui Province, ChinaResearch Institute of Donkey High-Efficiency Breeding and Ecological Feeding, College of Agronomy, Liaocheng University, Liaocheng 252000, Shandong Province, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, Anhui Province, ChinaBiotechnology Center, Anhui Agricultural University, Hefei 230036, Anhui Province, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, Anhui Province, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, Anhui Province, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, Anhui Province, ChinaCollege of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, Jiangsu Province, China; Corresponding authors.College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, Anhui Province, China; Corresponding authors.Nutrition consistently affects microbe-host interactions in the gastrointestinal tract. This study aimed to unravel how undernutrition reshapes the microbial composition and the homeostasis of epithelium in the jejunum and ileum. Sixteen late-gestation Hu-sheep were randomly assigned to the control group (n = 8, 100% ad libitum feeding levels) or the undernutrition group (n = 8, which received 30% ad libitum feeding levels). After 15-d treatment, all ewes were slaughtered, and jejunal and ileal digesta and epithelium samples were collected for 16S rRNA gene sequencing and transcriptome sequencing, respectively. Results indicated that undernutrition decreased the jejunal and ileal tissue weights (P = 0.005 and P = 0.022) and the levels of volatile fatty acids (P = 0.019 and P = 0.007) and microbial protein levels (P = 0.019 and P = 0.031) in jejunal and ileal digesta. The relative abundance of acetate producing microbiota, including Clostridia UCG-014 norank, Ruminococcus, [Ruminococcus] gauvreauii, and Lachnospiraceae_Blautia, were significantly reduced (P < 0.05) in the jejunum and ileum. Undernutrition up-regulated (P < 0.05) the expression of genes involved in amino acid synthesis and fatty acid oxidation, but down-regulated (P < 0.05) the expression of genes associated with amino acid degradation, fatty acid synthesis, and extracellular structures in jejunal and ileal epithelium. In the jejunal epithelium, genes associated with extracellular matrix–receptor interactions, cell growth, and immune response were down-regulated (P < 0.05) upon undernutrition. Taken together, undernutrition changed the microbial community in the jejunum and ileum, which altered the fermentation mode and the production of volatile fatty acids and microbial protein. These affected the energy and protein system in the epithelium and reprogrammed substance metabolism and extracellular structures, which probably further influenced cell growth and immune response. These insights provide a foundation for completely clarifying the crosstalk between small intestinal microbiota and the host.http://www.sciencedirect.com/science/article/pii/S2405654524001513UndernutritionMicrobiotaEpithelial metabolismImmune response
spellingShingle Weibin Wu
Muhammad Faheem Akhtar
Jiahong Geng
Huizhen Lu
Muhammad Ajwad Rahim
Jianbo Cheng
Xiaoling Ding
Shengyong Mao
Yanfeng Xue
Undernutrition disrupts jejunal and ileal microbiota and epithelial tissue homeostasis in a pregnant sheep model
Animal Nutrition
Undernutrition
Microbiota
Epithelial metabolism
Immune response
title Undernutrition disrupts jejunal and ileal microbiota and epithelial tissue homeostasis in a pregnant sheep model
title_full Undernutrition disrupts jejunal and ileal microbiota and epithelial tissue homeostasis in a pregnant sheep model
title_fullStr Undernutrition disrupts jejunal and ileal microbiota and epithelial tissue homeostasis in a pregnant sheep model
title_full_unstemmed Undernutrition disrupts jejunal and ileal microbiota and epithelial tissue homeostasis in a pregnant sheep model
title_short Undernutrition disrupts jejunal and ileal microbiota and epithelial tissue homeostasis in a pregnant sheep model
title_sort undernutrition disrupts jejunal and ileal microbiota and epithelial tissue homeostasis in a pregnant sheep model
topic Undernutrition
Microbiota
Epithelial metabolism
Immune response
url http://www.sciencedirect.com/science/article/pii/S2405654524001513
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