IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26209-8.html
   My bibliography  Save this article

High-coverage metabolomics uncovers microbiota-driven biochemical landscape of interorgan transport and gut-brain communication in mice

Author

Listed:
  • Yunjia Lai

    (Gillings School of Global Public Health, CB# 7431, University of North Carolina)

  • Chih-Wei Liu

    (Gillings School of Global Public Health, CB# 7431, University of North Carolina)

  • Yifei Yang

    (Gillings School of Global Public Health, CB# 7431, University of North Carolina)

  • Yun-Chung Hsiao

    (Gillings School of Global Public Health, CB# 7431, University of North Carolina)

  • Hongyu Ru

    (Gillings School of Global Public Health, CB# 7431, University of North Carolina)

  • Kun Lu

    (Gillings School of Global Public Health, CB# 7431, University of North Carolina)

Abstract

The mammalian gut harbors a complex and dynamic microbial ecosystem: the microbiota. While emerging studies support that microbiota regulates brain function with a few molecular cues suggested, the overall biochemical landscape of the “microbiota-gut-brain axis” remains largely unclear. Here we use high-coverage metabolomics to comparatively profile feces, blood sera, and cerebral cortical brain tissues of germ-free C57BL/6 mice and their age-matched conventionally raised counterparts. Results revealed for all three matrices metabolomic signatures owing to microbiota, yielding hundreds of identified metabolites including 533 altered for feces, 231 for sera, and 58 for brain with numerous significantly enriched pathways involving aromatic amino acids and neurotransmitters. Multicompartmental comparative analyses single out microbiota-derived metabolites potentially implicated in interorgan transport and the gut-brain axis, as exemplified by indoxyl sulfate and trimethylamine-N-oxide. Gender-specific characteristics of these landscapes are discussed. Our findings may be valuable for future research probing microbial influences on host metabolism and gut-brain communication.

Suggested Citation

  • Yunjia Lai & Chih-Wei Liu & Yifei Yang & Yun-Chung Hsiao & Hongyu Ru & Kun Lu, 2021. "High-coverage metabolomics uncovers microbiota-driven biochemical landscape of interorgan transport and gut-brain communication in mice," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26209-8
    DOI: 10.1038/s41467-021-26209-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26209-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-26209-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Peter J. Turnbaugh & Ruth E. Ley & Micah Hamady & Claire M. Fraser-Liggett & Rob Knight & Jeffrey I. Gordon, 2007. "The Human Microbiome Project," Nature, Nature, vol. 449(7164), pages 804-810, October.
    2. Peter J. Turnbaugh & Ruth E. Ley & Michael A. Mahowald & Vincent Magrini & Elaine R. Mardis & Jeffrey I. Gordon, 2006. "An obesity-associated gut microbiome with increased capacity for energy harvest," Nature, Nature, vol. 444(7122), pages 1027-1031, December.
    3. Coco Chu & Mitchell H. Murdock & Deqiang Jing & Tae Hyung Won & Hattie Chung & Adam M. Kressel & Tea Tsaava & Meghan E. Addorisio & Gregory G. Putzel & Lei Zhou & Nicholas J. Bessman & Ruirong Yang & , 2019. "The microbiota regulate neuronal function and fear extinction learning," Nature, Nature, vol. 574(7779), pages 543-548, October.
    4. Koichi Kikuchi & Daisuke Saigusa & Yoshitomi Kanemitsu & Yotaro Matsumoto & Paxton Thanai & Naoto Suzuki & Koki Mise & Hiroaki Yamaguchi & Tomohiro Nakamura & Kei Asaji & Chikahisa Mukawa & Hiroki Tsu, 2019. "Gut microbiome-derived phenyl sulfate contributes to albuminuria in diabetic kidney disease," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    5. Dylan Dodd & Matthew H. Spitzer & William Van Treuren & Bryan D. Merrill & Andrew J. Hryckowian & Steven K. Higginbottom & Anthony Le & Tina M. Cowan & Garry P. Nolan & Michael A. Fischbach & Justin L, 2017. "A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites," Nature, Nature, vol. 551(7682), pages 648-652, November.
    6. Alessia Visconti & Caroline I. Le Roy & Fabio Rosa & Niccolò Rossi & Tiphaine C. Martin & Robert P. Mohney & Weizhong Li & Emanuele Rinaldis & Jordana T. Bell & J. Craig Venter & Karen E. Nelson & Tim, 2019. "Interplay between the human gut microbiome and host metabolism," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Lixiang Zhai & Haitao Xiao & Chengyuan Lin & Hoi Leong Xavier Wong & Yan Y. Lam & Mengxue Gong & Guojun Wu & Ziwan Ning & Chunhua Huang & Yijing Zhang & Chao Yang & Jingyuan Luo & Lu Zhang & Ling Zhao, 2023. "Gut microbiota-derived tryptamine and phenethylamine impair insulin sensitivity in metabolic syndrome and irritable bowel syndrome," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Barbara Emmenegger & Julien Massoni & Christine M. Pestalozzi & Miriam Bortfeld-Miller & Benjamin A. Maier & Julia A. Vorholt, 2023. "Identifying microbiota community patterns important for plant protection using synthetic communities and machine learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Amirhossein Shamsaddini & Kimia Dadkhah & Patrick M Gillevet, 2020. "BiomMiner: An advanced exploratory microbiome analysis and visualization pipeline," PLOS ONE, Public Library of Science, vol. 15(6), pages 1-13, June.
    4. Rajita Menon & Vivek Ramanan & Kirill S Korolev, 2018. "Interactions between species introduce spurious associations in microbiome studies," PLOS Computational Biology, Public Library of Science, vol. 14(1), pages 1-20, January.
    5. Doratha A Byrd & Jun Chen & Emily Vogtmann & Autumn Hullings & Se Jin Song & Amnon Amir & Muhammad G Kibriya & Habibul Ahsan & Yu Chen & Heidi Nelson & Rob Knight & Jianxin Shi & Nicholas Chia & Rashm, 2019. "Reproducibility, stability, and accuracy of microbial profiles by fecal sample collection method in three distinct populations," PLOS ONE, Public Library of Science, vol. 14(11), pages 1-19, November.
    6. Shilan Li & Jianxin Shi & Paul Albert & Hong-Bin Fang, 2022. "Dependence Structure Analysis and Its Application in Human Microbiome," Mathematics, MDPI, vol. 11(1), pages 1-14, December.
    7. Daphna Rothschild & Erez Dekel & Jean Hausser & Anat Bren & Guy Aidelberg & Pablo Szekely & Uri Alon, 2014. "Linear Superposition and Prediction of Bacterial Promoter Activity Dynamics in Complex Conditions," PLOS Computational Biology, Public Library of Science, vol. 10(5), pages 1-9, May.
    8. Jae-Chang Cho, 2021. "Human microbiome privacy risks associated with summary statistics," PLOS ONE, Public Library of Science, vol. 16(4), pages 1-11, April.
    9. Kiran Konain & Sadia & Turfa Nadeem & Adeed Khan & Warda Iqbal & Arsalan & Amir Javed & Ruby Khan & Kainat Jamil & Kainat Jamil, 2018. "Importance of Probiotics in Gastrointestinal Tract," Journal of Asian Scientific Research, Asian Economic and Social Society, vol. 8(3), pages 128-143, March.
    10. Pirjo Wacklin & Harri Mäkivuokko & Noora Alakulppi & Janne Nikkilä & Heli Tenkanen & Jarkko Räbinä & Jukka Partanen & Kari Aranko & Jaana Mättö, 2011. "Secretor Genotype (FUT2 gene) Is Strongly Associated with the Composition of Bifidobacteria in the Human Intestine," PLOS ONE, Public Library of Science, vol. 6(5), pages 1-10, May.
    11. Marjolein Heddes & Baraa Altaha & Yunhui Niu & Sandra Reitmeier & Karin Kleigrewe & Dirk Haller & Silke Kiessling, 2022. "The intestinal clock drives the microbiome to maintain gastrointestinal homeostasis," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    12. Yee Sang Wong & Nicholas John Osborne, 2022. "Biodiversity Effects on Human Mental Health via Microbiota Alterations," IJERPH, MDPI, vol. 19(19), pages 1-13, September.
    13. Weiyue Ji & Handuo Shi & Haoqian Zhang & Rui Sun & Jingyi Xi & Dingqiao Wen & Jingchen Feng & Yiwei Chen & Xiao Qin & Yanrong Ma & Wenhan Luo & Linna Deng & Hanchi Lin & Ruofan Yu & Qi Ouyang, 2013. "A Formalized Design Process for Bacterial Consortia That Perform Logic Computing," PLOS ONE, Public Library of Science, vol. 8(2), pages 1-9, February.
    14. Shanguang Zhao & Selina Khoo & Siew-Cheok Ng & Aiping Chi, 2022. "Brain Functional Network and Amino Acid Metabolism Association in Females with Subclinical Depression," IJERPH, MDPI, vol. 19(6), pages 1-15, March.
    15. Disha Tandon & Mohammed Monzoorul Haque & Sharmila S Mande, 2016. "Inferring Intra-Community Microbial Interaction Patterns from Metagenomic Datasets Using Associative Rule Mining Techniques," PLOS ONE, Public Library of Science, vol. 11(4), pages 1-16, April.
    16. Eric Z. Chen & Frederic D. Bushman & Hongzhe Li, 2017. "A Model-Based Approach for Species Abundance Quantification Based on Shotgun Metagenomic Data," Statistics in Biosciences, Springer;International Chinese Statistical Association, vol. 9(1), pages 13-27, June.
    17. Melania Maria Serafini & Ambra Maddalon & Martina Iulini & Valentina Galbiati, 2022. "Air Pollution: Possible Interaction between the Immune and Nervous System?," IJERPH, MDPI, vol. 19(23), pages 1-24, November.
    18. Hui Xia & Beijia Zhou & Jing Sui & Wenqing Ma & Shaokang Wang & Ligang Yang & Guiju Sun, 2022. "Lycium barbarum Polysaccharide Regulates the Lipid Metabolism and Alters Gut Microbiota in High-Fat Diet Induced Obese Mice," IJERPH, MDPI, vol. 19(19), pages 1-12, September.
    19. Davillas, Apostolos & Pudney, Stephen, 2016. "Concordance of health states in couples. Analysis of self-reported, nurse administered and blood-based biomarker data in Understanding Society," ISER Working Paper Series 2016-15, Institute for Social and Economic Research.
    20. Vinod Nikhra, 2019. "Therapeutic Potential of Gut Microbiome Manipulation: Concepts in Fecal Microbiota Transplantation," Current Research in Diabetes & Obesity Journal, Juniper Publishers Inc., vol. 11(1), pages 1-9, June.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26209-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.