Early-life milk replacer feeding mediates lipid metabolism disorders induced by colonic microbiota and bile acid profiles to reduce body weight in goat model.

Bile acid Colon microbiota Goat model Lipid metabolism Milk replacer

Journal

Journal of animal science and biotechnology
ISSN: 1674-9782
Titre abrégé: J Anim Sci Biotechnol
Pays: England
ID NLM: 101581293

Informations de publication

Date de publication:
04 Sep 2024
Historique:
received: 06 05 2024
accepted: 30 06 2024
medline: 4 9 2024
pubmed: 4 9 2024
entrez: 3 9 2024
Statut: epublish

Résumé

Dysregulation of lipid metabolism and its consequences on growth performance in young ruminants have attracted attention, especially in the context of alternative feeding strategies. This study aims to elucidate the effects of milk replacer (MR) feeding on growth, lipid metabolism, colonic epithelial gene expression, colonic microbiota composition and systemic metabolism in goat kids compared to breast milk (BM) feeding, addressing a critical knowledge gap in early life nutrition. Ten female goat kids were divided into 2 groups: those fed breast milk (BM group) and those fed a milk replacer (MR group). Over a period of 28 d, body weight was monitored and blood and tissue samples were collected for biochemical, transcriptomic and metabolomic analyses. Profiling of the colonial microbiota was performed using 16S rRNA gene sequencing. Intestinal microbiota transplantation (IMT) experiments in gnotobiotic mice were performed to validate causality. MR-fed pups exhibited reduced daily body-weight gain due to impaired lipid metabolism as evidenced by lower serum and liver total cholesterol (TC) and non-esterified fatty acid (NEFA) concentrations. Transcriptomic analysis of the colonic epithelium revealed upregulated genes involved in negative regulation of lipid metabolism, concomitant with microbiota shifts characterized by a decrease in Firmicutes and an increase in Actinobacteria. Specifically, genera such as Bifidobacterium and Prevotella were enriched in the MR group, while Clostridium and Faecalibacterium were depleted. Metabolomics analyses confirmed alterations in bile acid and fatty acid metabolic pathways. IMT experiments in mice recapitulated the metabolic phenotype observed in MR-fed goats, confirming the role of the microbiota in modulating host lipid metabolism. Milk replacer feeding in goat kids disrupts lipid metabolism and gut microbiota dynamics, resulting in reduced growth rates and metabolic alterations. These findings highlight the importance of early nutritional intervention on metabolic programming and suggest that modulation of the gut microbiota may be a target for improving growth and metabolic health in ruminants. This study contributes to the understanding of nutritional management strategies in livestock and their impact on animal health and productivity.

Sections du résumé

BACKGROUND BACKGROUND
Dysregulation of lipid metabolism and its consequences on growth performance in young ruminants have attracted attention, especially in the context of alternative feeding strategies. This study aims to elucidate the effects of milk replacer (MR) feeding on growth, lipid metabolism, colonic epithelial gene expression, colonic microbiota composition and systemic metabolism in goat kids compared to breast milk (BM) feeding, addressing a critical knowledge gap in early life nutrition.
METHODS METHODS
Ten female goat kids were divided into 2 groups: those fed breast milk (BM group) and those fed a milk replacer (MR group). Over a period of 28 d, body weight was monitored and blood and tissue samples were collected for biochemical, transcriptomic and metabolomic analyses. Profiling of the colonial microbiota was performed using 16S rRNA gene sequencing. Intestinal microbiota transplantation (IMT) experiments in gnotobiotic mice were performed to validate causality.
RESULTS RESULTS
MR-fed pups exhibited reduced daily body-weight gain due to impaired lipid metabolism as evidenced by lower serum and liver total cholesterol (TC) and non-esterified fatty acid (NEFA) concentrations. Transcriptomic analysis of the colonic epithelium revealed upregulated genes involved in negative regulation of lipid metabolism, concomitant with microbiota shifts characterized by a decrease in Firmicutes and an increase in Actinobacteria. Specifically, genera such as Bifidobacterium and Prevotella were enriched in the MR group, while Clostridium and Faecalibacterium were depleted. Metabolomics analyses confirmed alterations in bile acid and fatty acid metabolic pathways. IMT experiments in mice recapitulated the metabolic phenotype observed in MR-fed goats, confirming the role of the microbiota in modulating host lipid metabolism.
CONCLUSIONS CONCLUSIONS
Milk replacer feeding in goat kids disrupts lipid metabolism and gut microbiota dynamics, resulting in reduced growth rates and metabolic alterations. These findings highlight the importance of early nutritional intervention on metabolic programming and suggest that modulation of the gut microbiota may be a target for improving growth and metabolic health in ruminants. This study contributes to the understanding of nutritional management strategies in livestock and their impact on animal health and productivity.

Identifiants

DOI: 10.1186/s40104-024-01072-x PMID: 39227902
pubmed: 39227902
doi: 10.1186/s40104-024-01072-x
pii: 10.1186/s40104-024-01072-x
doi:

Types de publication

Journal Article

Langues

eng

Pagination

118

Informations de copyright

© 2024. The Author(s).

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Auteurs

Ke Zhang (K)

Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China.

Ting Zhang (T)

Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China.

Mengmeng Guo (M)

College of Animal Engineering, Yangling Vocational and Technical College, Yangling , Shaanxi, 712100, China.

Awang Cuoji (A)

Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China.
Institute of Animal Sciences, Tibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, 850009, China.

Yangbin Xu (Y)

Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China.

Yitong Zhao (Y)

Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China.

Yuxin Yang (Y)

Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China.

Daniel Brugger (D)

Institute of Animal Nutrition and Dietetics, Vetsuisse-Faculty, University of Zurich, Zurich, 8057, Switzerland.

Xiaolong Wang (X)

Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China.

Langda Suo (L)

Institute of Animal Sciences, Tibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, 850009, China.
Key Laboratory of Animal Genetics and Breeding On Tibetan Plateau, Ministry of Agriculture and Rural Affairs, Lhasa, 850009, China.

Yujiang Wu (Y)

Institute of Animal Sciences, Tibet Academy of Agricultural and Animal Husbandry Sciences, Lhasa, 850009, China. wuyujiang_1979@163.com.
Key Laboratory of Animal Genetics and Breeding On Tibetan Plateau, Ministry of Agriculture and Rural Affairs, Lhasa, 850009, China. wuyujiang_1979@163.com.

Yulin Chen (Y)

Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China. chenyulin@nwafu.edu.cn.

Classifications MeSH