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Synergetic responses of intestinal microbiota and epithelium to dietary inulin supplementation in pigs

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Abstract

Purpose

Inulin is a soluble dietary fiber that has been implicated in regulating the intestinal health. Here, we describe a synergetic response of intestinal microbiota and epithelial functions to increased intake of inulin in a porcine model.

Methods

Twenty growing-pigs were randomly allocated to two groups (n = 10) and fed with a basal diet (BD) or BD containing 0.5% inulin (INU) for 21 days.

Results

We show that INU supplementation not only elevated villus height and the abundance of zonula occludens-1 (ZO-1), but also increased acetate and butyrate concentrations in cecum (P < 0.05). Moreover, INU decreased IL-6 and TNFα secretion, and reduced intestinal epithelial cell apoptosis in ileum and cecum (P < 0.05). Interestingly, we observed an elevated 16S rRNA gene copies in cecum after INU ingestion (P < 0.05). INU had no influence on overall diversity, but acutely altered the abundance of specific bacteria. INU decreased the abundance of phylum Proteobacteria in ileum, but increased the phylum Bacteroidetes in the ileum and cecum (P < 0.05). INU significantly elevated the Lactobacillus spp. and Bacteroides spp. in the ileum and cecum, respectively. Importantly, INU elevated the expression levels of GPR43, GLP-2, and ZO-1, but decreased the expression levels of histone deacetylase 1 (HDAC1) and TNFα in the ileum and cecum mucosa (P < 0.05). Moreover, INU also elevated the expression levels of GPR109A and angiopoietin-4 (ANG-4) in the cecum mucosa (P < 0.05).

Conclusions

This study indicated how the intestinal microbiome and epithelium adapt to inulin ingestion, and furthered our understanding of the mechanisms behind the dietary fiber-modulated intestinal microbiota and health.

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Availability of data and material

All sequencing information has been deposited in the National Center for Biotechnology Information (NCBI) and can be accessed in the Short Read Archie (SRA) under the accession number PRJNA559763.

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Acknowledgements

We thank Huifen Wang for technical help with the biochemical analysis. This study was supported by the National Natural Science Foundation of China (31972599) and the Development program of Sichuan Province (2018NZDZX0005).

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Author notes

  1. Jun He and Hongmei Xie contributed equally.

Authors and Affiliations

  1. Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, 611130, Sichuan, People’s Republic of China

    Jun He, Daiwen Chen, Bing Yu, Zhiqing Huang, Xiangbing Mao, Ping Zheng, Yuheng Luo, Jie Yu, Junqiu Luo & Hui Yan

  2. Key Laboratory of Animal Disease-Resistant Nutrition, Chengdu, 611130, Sichuan, People’s Republic of China

    Jun He, Daiwen Chen, Bing Yu, Zhiqing Huang, Xiangbing Mao, Ping Zheng, Yuheng Luo, Jie Yu, Junqiu Luo & Hui Yan

  3. Shandong Vocational Animal Science and Veterinary College, Weifang, 261061, Shandong, People’s Republic of China

    Hongmei Xie

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  1. Jun He
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Contributions

JH designed the experiments; WW and HX performed the animal trial and wrote the manuscript; PZ, JY, ZH, JL, and YL participated the biochemical assays; HY revised the manuscript. DC, BY, and XM conceived the experiment. All authors have read and approved the final draft.

Corresponding author

Correspondence to Jun He.

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Conflict of interest

The authors declare that they have no competing interests.

Ethics approval

Studies involving animals were conducted according to the Regulations for the Administration of Affairs Concerning Experimental Animals (Ministry of Science and Technology, China, revised in June 2004). Sample collection was approved by the Institutional Animal Care and Use Committee of Sichuan Agricultural University, Sichuan, China (no. 20180901).

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He, J., Xie, H., Chen, D. et al. Synergetic responses of intestinal microbiota and epithelium to dietary inulin supplementation in pigs. Eur J Nutr 60, 715–727 (2021). https://doi.org/10.1007/s00394-020-02284-3

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