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Richness of human gut microbiome correlates with metabolic markers

Author

Listed:
  • Emmanuelle Le Chatelier

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France)

  • Trine Nielsen

    (The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark)

  • Junjie Qin

    (BGI-Shenzhen)

  • Edi Prifti

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France)

  • Falk Hildebrand

    (VIB, Pleinlaan 2, 1050 Brussels, Belgium
    Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium)

  • Gwen Falony

    (VIB, Pleinlaan 2, 1050 Brussels, Belgium
    Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium)

  • Mathieu Almeida

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France)

  • Manimozhiyan Arumugam

    (The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark
    BGI-Shenzhen
    European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany)

  • Jean-Michel Batto

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France)

  • Sean Kennedy

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France)

  • Pierre Leonard

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France)

  • Junhua Li

    (BGI-Shenzhen
    School of Bioscience and Biotechnology, South China University of Technology)

  • Kristoffer Burgdorf

    (The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark)

  • Niels Grarup

    (The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark)

  • Torben Jørgensen

    (Research Centre for Prevention and Health, Glostrup University Hospital, DK-2900 Glostrup, Denmark
    Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark
    Institute of Public Health, Faculty of Medicine, University of Aalborg, DK-9100 Aalborg, Denmark)

  • Ivan Brandslund

    (Vejle Hospital, DK-7100 Vejle, Denmark
    Institute of Regional Health Research, University of Southern Denmark, DK-8200 Odense, Denmark)

  • Henrik Bjørn Nielsen

    (Center for Biological Sequence Analysis & Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark)

  • Agnieszka S. Juncker

    (Center for Biological Sequence Analysis & Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark)

  • Marcelo Bertalan

    (Center for Biological Sequence Analysis & Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark)

  • Florence Levenez

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France)

  • Nicolas Pons

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France)

  • Simon Rasmussen

    (Center for Biological Sequence Analysis & Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark)

  • Shinichi Sunagawa

    (European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany)

  • Julien Tap

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France
    European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany)

  • Sebastian Tims

    (Laboratory of Microbiology, Wageningen University, 6710BA Ede, The Netherlands)

  • Erwin G. Zoetendal

    (Laboratory of Microbiology, Wageningen University, 6710BA Ede, The Netherlands)

  • Søren Brunak

    (Center for Biological Sequence Analysis & Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark)

  • Karine Clément

    (Institut National de la Santé et de la Recherche Médicale, U 872, Nutriomique, Équipe 7, Centre de Recherches des Cordeliers, 75006 Paris, France
    Université Pierre et Marie-Curie-Paris VI, 75006 Paris, France
    Assistance Publique-Hôpitaux de Paris, Institute of Cardiometabolism and Nutrition, CRNH-Ile de France, Pitié-Salpêtrière, 75013 Paris, France)

  • Joël Doré

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France
    INRA, Institut National de la Recherche Agronomique, UMR 14121 MICALIS, 78350 Jouy en Josas, France)

  • Michiel Kleerebezem

    (Laboratory of Microbiology, Wageningen University, 6710BA Ede, The Netherlands)

  • Karsten Kristiansen

    (Ole Maaløes Vej 5, University of Copenhagen, DK-2200 Copenhagen, Denmark)

  • Pierre Renault

    (INRA, Institut National de la Recherche Agronomique, UMR 14121 MICALIS, 78350 Jouy en Josas, France)

  • Thomas Sicheritz-Ponten

    (Center for Biological Sequence Analysis & Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark)

  • Willem M. de Vos

    (Laboratory of Microbiology, Wageningen University, 6710BA Ede, The Netherlands
    University of Helsinki, FIN-00014 Finland)

  • Jean-Daniel Zucker

    (Institut National de la Santé et de la Recherche Médicale, U 872, Nutriomique, Équipe 7, Centre de Recherches des Cordeliers, 75006 Paris, France
    Université Pierre et Marie-Curie-Paris VI, 75006 Paris, France
    Institut de Recherche pour le Développement, UMI 209, Unité de modélisation mathématique et informatique des Systèmes Complexes, F-93143 Bondy, France)

  • Jeroen Raes

    (VIB, Pleinlaan 2, 1050 Brussels, Belgium
    Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium)

  • Torben Hansen

    (The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark
    Faculty of Health Sciences, University of Southern Denmark, DK-8200 Odense, Denmark)

  • Peer Bork

    (European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany)

  • Jun Wang

    (BGI-Shenzhen
    Ole Maaløes Vej 5, University of Copenhagen, DK-2200 Copenhagen, Denmark
    King Abdulazziz University, Jeddah 21589, Saudi Arabia
    Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, DK-2200 Copenhagen, Denmark)

  • S. Dusko Ehrlich

    (INRA, Institut National de la Recherche Agronomique, US1367 Metagenopolis, 78350 Jouy en Josas, France)

  • Oluf Pedersen

    (The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark
    Hagedorn Research Institute, DK-2820 Gentofte, Denmark
    Institute of Biomedical Science, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark
    Faculty of Health, Aarhus University, DK-8000 Aarhus, Denmark)

Abstract

We are facing a global metabolic health crisis provoked by an obesity epidemic. Here we report the human gut microbial composition in a population sample of 123 non-obese and 169 obese Danish individuals. We find two groups of individuals that differ by the number of gut microbial genes and thus gut bacterial richness. They contain known and previously unknown bacterial species at different proportions; individuals with a low bacterial richness (23% of the population) are characterized by more marked overall adiposity, insulin resistance and dyslipidaemia and a more pronounced inflammatory phenotype when compared with high bacterial richness individuals. The obese individuals among the lower bacterial richness group also gain more weight over time. Only a few bacterial species are sufficient to distinguish between individuals with high and low bacterial richness, and even between lean and obese participants. Our classifications based on variation in the gut microbiome identify subsets of individuals in the general white adult population who may be at increased risk of progressing to adiposity-associated co-morbidities.

Suggested Citation

  • Emmanuelle Le Chatelier & Trine Nielsen & Junjie Qin & Edi Prifti & Falk Hildebrand & Gwen Falony & Mathieu Almeida & Manimozhiyan Arumugam & Jean-Michel Batto & Sean Kennedy & Pierre Leonard & Junhua, 2013. "Richness of human gut microbiome correlates with metabolic markers," Nature, Nature, vol. 500(7464), pages 541-546, August.
  • Handle: RePEc:nat:nature:v:500:y:2013:i:7464:d:10.1038_nature12506
    DOI: 10.1038/nature12506
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    Cited by:

    1. Qiwen Cheng & Rosa Krajmalnik-Brown & John K. DiBaise & Juan Maldonado & M. Aaron Guest & Michael Todd & Shelby L. Langer, 2023. "Relationship Functioning and Gut Microbiota Composition among Older Adult Couples," IJERPH, MDPI, vol. 20(8), pages 1-17, April.
    2. Alessandra N. Bazzano & Kaitlin S. Potts & Lydia A. Bazzano & John B. Mason, 2017. "The Life Course Implications of Ready to Use Therapeutic Food for Children in Low-Income Countries," IJERPH, MDPI, vol. 14(4), pages 1-19, April.
    3. Jim Parker & Claire O’Brien & Jason Hawrelak & Felice L. Gersh, 2022. "Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment," IJERPH, MDPI, vol. 19(3), pages 1-25, January.
    4. Patricia A. Janulewicz & Ratanesh K. Seth & Jeffrey M. Carlson & Joy Ajama & Emily Quinn & Timothy Heeren & Nancy Klimas & Steven M. Lasley & Ronnie D. Horner & Kimberly Sullivan & Saurabh Chatterjee, 2019. "The Gut-Microbiome in Gulf War Veterans: A Preliminary Report," IJERPH, MDPI, vol. 16(19), pages 1-14, October.
    5. Małgorzata Moszak & Monika Szulińska & Marta Walczak-Gałęzewska & Paweł Bogdański, 2021. "Nutritional Approach Targeting Gut Microbiota in NAFLD—To Date," IJERPH, MDPI, vol. 18(4), pages 1-32, February.
    6. Natalia Di Tommaso & Antonio Gasbarrini & Francesca Romana Ponziani, 2021. "Intestinal Barrier in Human Health and Disease," IJERPH, MDPI, vol. 18(23), pages 1-23, December.
    7. Zhibo Xie & Yuning Sun & Yuqian Ye & Dandan Hu & Hua Zhang & Zhangyuting He & Haitao Zhao & Huayu Yang & Yilei Mao, 2022. "Randomized controlled trial for time-restricted eating in healthy volunteers without obesity," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    8. Lauren C Mead & Alison M Hill & Sharayah Carter & Alison M Coates, 2021. "The Effect of Nut Consumption on Diet Quality, Cardiometabolic and Gastrointestinal Health in Children: A Systematic Review of Randomized Controlled Trials," IJERPH, MDPI, vol. 18(2), pages 1-15, January.
    9. Zengliang Jiang & Lai-bao Zhuo & Yan He & Yuanqing Fu & Luqi Shen & Fengzhe Xu & Wanglong Gou & Zelei Miao & Menglei Shuai & Yuhui Liang & Congmei Xiao & Xinxiu Liang & Yunyi Tian & Jiali Wang & Jun T, 2022. "The gut microbiota-bile acid axis links the positive association between chronic insomnia and cardiometabolic diseases," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    10. Alvah Zorea & David Pellow & Liron Levin & Shai Pilosof & Jonathan Friedman & Ron Shamir & Itzhak Mizrahi, 2024. "Plasmids in the human gut reveal neutral dispersal and recombination that is overpowered by inflammatory diseases," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    11. Sigal Leviatan & Saar Shoer & Daphna Rothschild & Maria Gorodetski & Eran Segal, 2022. "An expanded reference map of the human gut microbiome reveals hundreds of previously unknown species," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    12. Julien Tap & Franck Lejzerowicz & Aurélie Cotillard & Matthieu Pichaud & Daniel McDonald & Se Jin Song & Rob Knight & Patrick Veiga & Muriel Derrien, 2023. "Global branches and local states of the human gut microbiome define associations with environmental and intrinsic factors," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    13. Alba Ordoñez-Rodriguez & Pablo Roman & Lola Rueda-Ruzafa & Ana Campos-Rios & Diana Cardona, 2023. "Changes in Gut Microbiota and Multiple Sclerosis: A Systematic Review," IJERPH, MDPI, vol. 20(5), pages 1-16, March.
    14. Gertrude Ecklu-Mensah & Candice Choo-Kang & Maria Gjerstad Maseng & Sonya Donato & Pascal Bovet & Bharathi Viswanathan & Kweku Bedu-Addo & Jacob Plange-Rhule & Prince Oti Boateng & Terrence E. Forrest, 2023. "Gut microbiota and fecal short chain fatty acids differ with adiposity and country of origin: the METS-microbiome study," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. Daphna Rothschild & Sigal Leviatan & Ariel Hanemann & Yossi Cohen & Omer Weissbrod & Eran Segal, 2022. "An atlas of robust microbiome associations with phenotypic traits based on large-scale cohorts from two continents," PLOS ONE, Public Library of Science, vol. 17(3), pages 1-20, March.

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