Abstract

The host genome may influence the composition of the intestinal microbiota, and the intestinal microbiota has a significant effect on muscle growth and development. In this study, we found that the deletion of the myostatin (MSTN) gene positively regulates the expression of the intestinal tight junction-related genes TJP1 and OCLN through the myosin light-chain kinase/myosin light chain pathway. The intestinal structure of MSTN−/− pigs differed from wild-type, including by the presence of a thicker muscularis and longer plicae. Together, these changes affect the structure of intestinal microbiota. Mice transplanted with the intestinal microbiota of MSTN−/− pigs had myofibers with larger cross-sectional areas and higher fast-twitch glycolytic muscle mass. Microbes responsible for the production of short-chain fatty acids (SCFAs) were enriched in both the MSTN−/− pigs and recipient mice, and SCFAs levels were elevated in the colon contents. We also demonstrated that valeric acid stimulates type IIb myofiber growth by activating the Akt/mTOR pathway via G protein-coupled receptor 43 and ameliorates dexamethasone-induced muscle atrophy. This is the first study to identify the MSTN gene-gut microbiota-SCFA axis and its regulatory role in fast-twitch glycolytic muscle growth.

Data availability

The raw reads of 16s rRNA gene sequences have been submitted to the NCBI BioSample database (Porcine data: PRJNA743164; Mice data: PRJNA743401).

The following data sets were generated
    1. Luo ZB
    (2022) Original data of Luo et al
    Science Data Bank, doi:10.57760/sciencedb.06767.

Article and author information

Author details

  1. Zhao-Bo Luo

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Shengzhong Han

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Xi-Jun Yin

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Hongye Liu

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Junxia Wang

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Meifu Xuan

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Chunyun Hao

    College of Integration Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Danqi Wang

    College of Integration Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0009-0001-7656-9901
  9. Yize Liu

    Key Laboratory of Natural Medicines of the Changbai Mountain, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Shuangyan Chang

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Dongxu Li

    College of Integration Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Kai Gao

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Huiling Li

    Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Biaohu Quan

    Department of Animal Science, Yanbian University, Yanji, China
    Competing interests
    The authors declare that no competing interests exist.
  15. Lin-Hu Quan

    Key Laboratory of Natural Medicines of the Changbai Mountain, Yanbian University, Yanji, China
    For correspondence
    lhquan@ybu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7195-8078
  16. Jin-Dan Kang

    Department of Animal Science, Yanbian University, Yanji, China
    For correspondence
    jdkang@ybu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Natural Science Foundation of China (32260817)

  • Jin-Dan Kang

National Natural Science Foundation of China (32260026)

  • Lin-Hu Quan

Changbai Mountain Talent Project of Jilin Province (000007)

  • Lin-Hu Quan

Higher Education Discipline Innovation Project (D18012)

  • Lin-Hu Quan

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: The animal study was approved by the Ethics Committee of Yanbian University (approval number SYXK2020-0009).

Copyright

© 2023, Luo et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,392
    views
  • 325
    downloads
  • 10
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Zhao-Bo Luo
  2. Shengzhong Han
  3. Xi-Jun Yin
  4. Hongye Liu
  5. Junxia Wang
  6. Meifu Xuan
  7. Chunyun Hao
  8. Danqi Wang
  9. Yize Liu
  10. Shuangyan Chang
  11. Dongxu Li
  12. Kai Gao
  13. Huiling Li
  14. Biaohu Quan
  15. Lin-Hu Quan
  16. Jin-Dan Kang
(2023)
Fecal transplant from myostatin deletion pigs positively impacts the gut-muscle axis
eLife 12:e81858.
https://doi.org/10.7554/eLife.81858

Share this article

https://doi.org/10.7554/eLife.81858

Further reading

    1. Developmental Biology
    2. Neuroscience
    Taro Ichimura, Taishi Kakizuka ... Takeharu Nagai
    Tools and Resources

    We established a volumetric trans-scale imaging system with an ultra-large field-of-view (FOV) that enables simultaneous observation of millions of cellular dynamics in centimeter-wide three-dimensional (3D) tissues and embryos. Using a custom-made giant lens system with a magnification of ×2 and a numerical aperture (NA) of 0.25, and a CMOS camera with more than 100 megapixels, we built a trans-scale scope AMATERAS-2, and realized fluorescence imaging with a transverse spatial resolution of approximately 1.1 µm across an FOV of approximately 1.5×1.0 cm2. The 3D resolving capability was realized through a combination of optical and computational sectioning techniques tailored for our low-power imaging system. We applied the imaging technique to 1.2 cm-wide section of mouse brain, and successfully observed various regions of the brain with sub-cellular resolution in a single FOV. We also performed time-lapse imaging of a 1-cm-wide vascular network during quail embryo development for over 24 hr, visualizing the movement of over 4.0×105 vascular endothelial cells and quantitatively analyzing their dynamics. Our results demonstrate the potential of this technique in accelerating production of comprehensive reference maps of all cells in organisms and tissues, which contributes to understanding developmental processes, brain functions, and pathogenesis of disease, as well as high-throughput quality check of tissues used for transplantation medicine.

    1. Developmental Biology
    2. Evolutionary Biology
    Hope M Healey, Hayden B Penn ... William A Cresko
    Research Article

    Seahorses, pipefishes, and seadragons are fishes from the family Syngnathidae that have evolved extraordinary traits including male pregnancy, elongated snouts, loss of teeth, and dermal bony armor. The developmental genetic and cellular changes that led to the evolution of these traits are largely unknown. Recent syngnathid genome assemblies revealed suggestive gene content differences and provided the opportunity for detailed genetic analyses. We created a single-cell RNA sequencing atlas of Gulf pipefish embryos to understand the developmental basis of four traits: derived head shape, toothlessness, dermal armor, and male pregnancy. We completed marker gene analyses, built genetic networks, and examined the spatial expression of select genes. We identified osteochondrogenic mesenchymal cells in the elongating face that express regulatory genes bmp4, sfrp1a, and prdm16. We found no evidence for tooth primordia cells, and we observed re-deployment of osteoblast genetic networks in developing dermal armor. Finally, we found that epidermal cells expressed nutrient processing and environmental sensing genes, potentially relevant for the brooding environment. The examined pipefish evolutionary innovations are composed of recognizable cell types, suggesting that derived features originate from changes within existing gene networks. Future work addressing syngnathid gene networks across multiple stages and species is essential for understanding how the novelties of these fish evolved.