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Translocation of gut microbes to epididymal white adipose tissue drives lipid metabolism disorder under heat stress

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Abstract

Heat stress induces multi-organ damage and serious physiological dysfunction in mammals, and gut bacteria may translocate to extra-intestinal tissues under heat stress pathology. However, whether gut bacteria translocate to the key metabolic organs and impair function as a result of heat stress remains unknown. Using a heat stress-induced mouse model, heat stress inhibited epididymal white adipose tissue (eWAT) expansion and induced lipid metabolic disorder but did not damage other organs, such as the heart, liver, spleen, or muscle. Microbial profiling analysis revealed that heat stress shifted the bacterial community in the cecum and eWAT but not in the inguinal white adipose tissue, blood, heart, liver, spleen, or muscle. Notably, gut-vascular barrier function was impaired, and the levels of some bacteria, particularly Lactobacillus, were higher in the eWAT, as confirmed by catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH) staining when mice were under heat stress. Moreover, integrated multi-omics analysis showed that the eWAT microbiota was associated with host lipid metabolism, and the expression of genes involved in the lipid metabolism in eWAT was upregulated under heat stress. A follow-up microbial supplementation study after introducing Lactobacillus plantarum to heat-stressed mice revealed that the probiotic ameliorated heat stress-induced loss of eWAT and dyslipidemia and reduced gut bacterial translocation to the eWAT by improving gut barrier function. Overall, our findings suggest that gut bacteria, particularly Lactobacillus spp., play a crucial role in heat stress-induced lipid metabolism disorder and that there is therapeutic potential for using probiotics, such as Lactobacillus plantarum.

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Acknowledgements

This work was supported in part by the National Key Research and Development Program of China Project (2022YFD1300402), fundamental research funds for the Central Universities (2662022DKPY004, 2662023DKPY002), and the Top-Notch Young Talent Supporting Program (to LH Sun).

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Author notes

  1. Contributed equally to this work

Authors and Affiliations

  1. State Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China

    Zhang-Chao Deng, Jia-Cheng Yang, Yu-Xuan Huang, Ling Zhao, Jinshui Zheng, Qing-Biao Xu & Lv-Hui Sun

  2. Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, T6G 2P5, Canada

    Leluo Guan

Authors
  1. Zhang-Chao Deng
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  2. Jia-Cheng Yang
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  3. Yu-Xuan Huang
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  4. Ling Zhao
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  5. Jinshui Zheng
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  6. Qing-Biao Xu
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  7. Leluo Guan
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  8. Lv-Hui Sun
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Corresponding author

Correspondence to Lv-Hui Sun.

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Compliance and ethics The author(s) declare that they have no conflict of interest.

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Deng, ZC., Yang, JC., Huang, YX. et al. Translocation of gut microbes to epididymal white adipose tissue drives lipid metabolism disorder under heat stress. Sci. China Life Sci. 66, 2877–2895 (2023). https://doi.org/10.1007/s11427-022-2320-y

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  • DOI: https://doi.org/10.1007/s11427-022-2320-y

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