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Role of iron in host-microbiota interaction and its effects on intestinal mucosal growth and immune plasticity in a piglet model

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Abstract

Iron is an essential trace element for both the host and resident microbes in the gut. In this study, iron was administered orally and parenterally to anemic piglets to investigate the role of iron in host-microbiota interaction and its effects on intestinal mucosal growth and immune plasticity. We found that oral iron administration easily increased the abundance of Proteobacteria and Escherichia-Shigella, and decreased the abundance of Lactobacillus in the ileum. Furthermore, similar bacterial changes, namely an increase in Proteobacteria, Escherichia-Shigella, and Fusobacterium and a reduction in the Christensenellaceae_R-7_group, were observed in the colon of both iron-supplemented groups. Spearman’s correlation analysis indicated that the changed Fusobacterium, Fusobacteria and Proteobacteria in the colon were positively correlated with hemoglobin, colon and spleen iron levels. Nevertheless, it was found that activated mTOR1 signaling, improved villous height and crypt depth in the ileum, enhanced immune communication, and increased protein expression of IL-22 and IL-10 in the colon of both iron-supplemented groups. In conclusion, the benefits of improved host iron outweigh the risks of altered gut microbiota for intestinal mucosal growth and immune regulation in treating iron deficiency anemia.

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Acknowledgements

This work was supported by the Natural Science Foundation of Hunan Province (2020JJ5635), Youth Innovation Promotion Association of Chinese Academy of Sciences (2022370), the National Center of Technology Innovation for pigs, the Science and Technology Program of Hunan Province (2020NK2013, 2020GK4095), Outstanding Youth Fund of Hunan Natural Science Foundation (2021JJ20045), the Key R&D Program of Guangxi Province (2021AB20063), the National Natural Science Foundation of China (32130099) and the China Agriculture Research System of MOF and MARA (CARS-35).

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Authors and Affiliations

  1. Key Laboratory of Agro-Ecological Processes in Subtropical Region, Hunan Research Center of Livestock & Poultry Sciences, South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China

    Zhenglin Dong, Shuan Liu, Yulong Tang, Xin Wu, Dan Wan & Yulong Yin

  2. Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Laboratory of Animal Nutrition and Human Health, College of Life Sciences, Hunan Normal University, Changsha, 410081, China

    Qingqing Deng & Guanya Li

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  1. Zhenglin Dong
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  2. Shuan Liu
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  3. Qingqing Deng
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  4. Guanya Li
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  5. Yulong Tang
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  6. Xin Wu
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  7. Dan Wan
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  8. Yulong Yin
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Correspondence to Dan Wan or Yulong Yin.

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Dong, Z., Liu, S., Deng, Q. et al. Role of iron in host-microbiota interaction and its effects on intestinal mucosal growth and immune plasticity in a piglet model. Sci. China Life Sci. 66, 2086–2098 (2023). https://doi.org/10.1007/s11427-022-2409-0

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