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Acetate reprograms gut microbiota during alcohol consumption

Author

Listed:
  • Cameron Martino

    (University of California San Diego
    University of California San Diego
    University of California San Diego)

  • Livia S. Zaramela

    (University of California San Diego)

  • Bei Gao

    (University of California San Diego)

  • Mallory Embree

    (University of California)

  • Janna Tarasova

    (University of California San Diego)

  • Seth J. Parker

    (University of California)

  • Yanhan Wang

    (University of California San Diego)

  • Huikuan Chu

    (University of California San Diego)

  • Peng Chen

    (University of California San Diego)

  • Kuei-Chuan Lee

    (University of California San Diego)

  • Daniela Domingos Galzerani

    (University of California San Diego)

  • Jivani M. Gengatharan

    (University of California
    The Salk Institute for Biological Studies)

  • Asama Lekbua

    (University of California San Diego)

  • Maxwell Neal

    (University of California San Diego)

  • Rob Knight

    (University of California San Diego
    University of California San Diego
    University of California
    University of California San Diego)

  • Hidekazu Tsukamoto

    (Southern California Research Center for ALPD and Cirrhosis and Department of Pathology
    Department of Veterans Affairs Greater Los Angeles Healthcare System)

  • Christian M. Metallo

    (University of California
    The Salk Institute for Biological Studies)

  • Bernd Schnabl

    (University of California San Diego
    University of California San Diego
    VA San Diego Healthcare System)

  • Karsten Zengler

    (University of California San Diego
    University of California San Diego
    University of California)

Abstract

Liver damage due to chronic alcohol use is among the most prevalent liver diseases. Alcohol consumption frequency is a strong factor of microbiota variance. Here we use isotope labeled [1-13C] ethanol, metagenomics, and metatranscriptomics in ethanol-feeding and intragastric mouse models to investigate the metabolic impacts of alcohol consumption on the gut microbiota. First, we show that although stable isotope labeled [1-13C] ethanol contributes to fatty acid pools in the liver, plasma, and cecum contents of mice, there is no evidence of ethanol metabolism by gut microbiota ex vivo under anaerobic conditions. Next, we observe through metatranscriptomics that the gut microbiota responds to ethanol-feeding by activating acetate dissimilation, not by metabolizing ethanol directly. We demonstrate that blood acetate concentrations are elevated during ethanol consumption. Finally, by increasing systemic acetate levels with glyceryl triacetate supplementation, we do not observe any impact on liver disease, but do induce similar gut microbiota alterations as chronic ethanol-feeding in mice. Our results show that ethanol is not directly metabolized by the gut microbiota, and changes in the gut microbiota linked to ethanol are a side effect of elevated acetate levels. De-trending for these acetate effects may be critical for understanding gut microbiota changes that cause alcohol-related liver disease.

Suggested Citation

  • Cameron Martino & Livia S. Zaramela & Bei Gao & Mallory Embree & Janna Tarasova & Seth J. Parker & Yanhan Wang & Huikuan Chu & Peng Chen & Kuei-Chuan Lee & Daniela Domingos Galzerani & Jivani M. Genga, 2022. "Acetate reprograms gut microbiota during alcohol consumption," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31973-2
    DOI: 10.1038/s41467-022-31973-2
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    References listed on IDEAS

    as
    1. Yi Duan & Cristina Llorente & Sonja Lang & Katharina Brandl & Huikuan Chu & Lu Jiang & Richard C. White & Thomas H. Clarke & Kevin Nguyen & Manolito Torralba & Yan Shao & Jinyuan Liu & Adriana Hernand, 2019. "Bacteriophage targeting of gut bacterium attenuates alcoholic liver disease," Nature, Nature, vol. 575(7783), pages 505-511, November.
    2. Ivan Vujkovic-Cvijin & Jack Sklar & Lingjing Jiang & Loki Natarajan & Rob Knight & Yasmine Belkaid, 2020. "Host variables confound gut microbiota studies of human disease," Nature, Nature, vol. 587(7834), pages 448-454, November.
    3. Francesco Asnicar & Andrew Maltez Thomas & Francesco Beghini & Claudia Mengoni & Serena Manara & Paolo Manghi & Qiyun Zhu & Mattia Bolzan & Fabio Cumbo & Uyen May & Jon G. Sanders & Moreno Zolfo & Evg, 2020. "Precise phylogenetic analysis of microbial isolates and genomes from metagenomes using PhyloPhlAn 3.0," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    4. Kristoffer Forslund & Falk Hildebrand & Trine Nielsen & Gwen Falony & Emmanuelle Le Chatelier & Shinichi Sunagawa & Edi Prifti & Sara Vieira-Silva & Valborg Gudmundsdottir & Helle Krogh Pedersen & Man, 2015. "Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota," Nature, Nature, vol. 528(7581), pages 262-266, December.
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