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Enterotypes of the human gut microbiome

Nature volume 473, pages 174–180 (2011)Cite this article

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An Addendum to this article was published on 26 February 2014

A Corrigendum to this article was published on 08 June 2011

This article has been updated

Abstract

Our knowledge of species and functional composition of the human gut microbiome is rapidly increasing, but it is still based on very few cohorts and little is known about variation across the world. By combining 22 newly sequenced faecal metagenomes of individuals from four countries with previously published data sets, here we identify three robust clusters (referred to as enterotypes hereafter) that are not nation or continent specific. We also confirmed the enterotypes in two published, larger cohorts, indicating that intestinal microbiota variation is generally stratified, not continuous. This indicates further the existence of a limited number of well-balanced host–microbial symbiotic states that might respond differently to diet and drug intake. The enterotypes are mostly driven by species composition, but abundant molecular functions are not necessarily provided by abundant species, highlighting the importance of a functional analysis to understand microbial communities. Although individual host properties such as body mass index, age, or gender cannot explain the observed enterotypes, data-driven marker genes or functional modules can be identified for each of these host properties. For example, twelve genes significantly correlate with age and three functional modules with the body mass index, hinting at a diagnostic potential of microbial markers.

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Figure 1: Functional and phylogenetic profiles of human gut microbiome.
Figure 2: Phylogenetic differences between enterotypes.
Figure 3: Functional differences between enterotypes.
Figure 4: Correlations with host properties.

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  • 08 June 2011

    An author was omitted. His name has been added to the HTML and PDF and described in the accompanying Corrigendum.

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Acknowledgements

The authors are grateful to C. Creevey, G. Falony and members of the Bork group at EMBL for discussions and assistance. We thank the EMBL IT core facility and Y. Yuan for managing the high-performance computing resources. The research leading to these results has received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013): MetaHIT, grant agreement HEALTH-F4-2007-201052, EMBL, the Lundbeck Foundation Centre for Applied Medical Genomics in Personalized Disease Prediction, Prevention and Care (LuCAMP), Novo Nordisk Foundation and the International Science and Technology Cooperation Project in China (0806). Obese/non-obese volunteers for the MicroObes study were recruited from the SU.VI.MAX cohort study coordinated by P. Galan and S. Hercberg, and metagenome sequencing was funded by Agence Nationale de la Recherche (ANR); volunteers for MicroAge study were recruited from the CROWNALIFE cohort study coordinated by S. Silvi and A. Cresci, and metagenome sequencing was funded by GenoScope. Ciberehd is funded by the Instituto de Salud Carlos III (Spain). J.R. is supported by the Institute for the encouragement of Scientific Research and Innovation of Brussels (ISRIB) and the Odysseus programme of the Fund for Scientific Research Flanders (FWO). We are thankful to the Human Microbiome Project for generating the reference genomes from human gut microbes and the International Human Microbiome Consortium for discussions and exchange of data.

Author information

Author notes

  1. Manimozhiyan Arumugam and Jeroen Raes: These authors contributed equally to this work.

Authors and Affiliations

  1. European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany

    Manimozhiyan Arumugam, Jeroen Raes, Takuji Yamada, Daniel R. Mende, Gabriel R. Fernandes, Julien Tap & Peer Bork

  2. VIB—Vrije Universiteit Brussel, 1050 Brussels, Belgium

    Jeroen Raes

  3. Commissariat à l’Energie Atomique, Genoscope, 91000 Evry, France

    Eric Pelletier, Denis Le Paslier, Thomas Bruls, Julie Poulain, Edgardo Ugarte & Jean Weissenbach

  4. Centre National de la Recherche Scientifique, UMR8030, 91000 Evry, France

    Eric Pelletier, Denis Le Paslier, Thomas Bruls & Jean Weissenbach

  5. Université d'Evry Val d'Essone 91000 Evry, France

    Eric Pelletier, Denis Le Paslier, Thomas Bruls & Jean Weissenbach

  6. Department of Biochemistry and Immunology, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, 31270-901 Belo Horizonte, Minas Gerais, Brazil

    Gabriel R. Fernandes

  7. Institut National de la Recherche Agronomique, 78350 Jouy en Josas, France

    Julien Tap, Jean-Michel Batto, Marion Leclerc, Florence Levenez, Nicolas Pons, Joel Doré & S. Dusko Ehrlich

  8. Center for Biological Sequence Analysis, Technical University of Denmark, DK-2800 Lyngby, Denmark

    Marcelo Bertalan, Laurent Gautier, H. Bjørn Nielsen, Thomas Sicheritz-Ponten & Søren Brunak

  9. Digestive System Research Unit, University Hospital Vall d’Hebron, Ciberehd, 08035 Barcelona, Spain

    Natalia Borruel, Francesc Casellas, Chaysavanh Manichanh & Francisco Guarner

  10. Barcelona Supercomputing Center, Jordi Girona 31, 08034 Barcelona, Spain

    Leyden Fernandez & David Torrents

  11. Marie Krogh Center for Metabolic Research, Section of Metabolic Genetics, Faculty of Health Sciences, University of Copenhagen, DK-2100 Copenhagen, Denmark

    Torben Hansen, Trine Nielsen & Oluf Pedersen

  12. Faculty of Health Sciences, University of Southern Denmark, DK-5000 Odense, Denmark

    Torben Hansen

  13. Computational Biology Laboratory Bld, The University of Tokyo Kashiwa Campus, Kashiwa-no-ha 5-1-5, Kashiwa, Chiba, 277-8561, Japan

    Masahira Hattori

  14. Division of Bioenvironmental Science, Frontier Science Research Center, University of Miyazaki, 5200 Kiyotake, Miyazaki 889-1692, Japan

    Tetsuya Hayashi

  15. Laboratory of Microbiology, Wageningen University, 6710BA Ede, The Netherlands

    Michiel Kleerebezem, Sebastian Tims, Erwin G. Zoetendal & Willem M. de Vos

  16. Department of Biological Information, Tokyo Institute of Technology, Graduate School of Bioscience and Biotechnology, 4259 Nagatsuta-cho, Midori-ku, Yokohama-shi, Kanagawa Pref. 226-8501, Japan

    Ken Kurokawa

  17. BGI-Shenzhen, Shenzhen, 518083, China

    Junjie Qin & Jun Wang

  18. Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, DK-2800 Lyngby, Denmark

    Thomas Sicheritz-Ponten

  19. Institució Catalana de Recerca i Estudis Avançats (ICREA), Pg. Lluís Companys 23, 08010 Barcelona, Spain

    David Torrents

  20. Department of Biology, University of Copenhagen, DK-2200 Copenhagen, Denmark

    Jun Wang

  21. Institute of Biomedical Science, Faculty of Health Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark

    Oluf Pedersen

  22. Hagedorn Research Institute, DK-2820 Gentofte, Denmark

    Oluf Pedersen

  23. Faculty of Health Sciences, University of Aarhus, DK-8000 Aarhus, Denmark

    Oluf Pedersen

  24. University of Helsinki, FI-00014 Helsinki, Finland

    Willem M. de Vos

  25. Max Delbrück Centre for Molecular Medicine, D-13092 Berlin, Germany

    Peer Bork

  26. Digestive System Research Unit, University Hospital Vall d’Hebron, Ciberehd, 08035 Barcelona, Spain

    María Antolín, Antonio Torrejon & Encarna Varela

  27. Commissariat à l’Energie Atomique, Genoscope, 91000 Evry, France

    François Artiguenave & Raquel Melo Minardi

  28. Institut National de la Recherche Agronomique, 78350 Jouy en Josas, France

    Hervé M. Blottiere, Mathieu Almeida, Antonella Cultrone, Christine Delorme, Rozenn Dervyn, Maarten van de Guchte, Eric Guedon, Florence Haimet, Alexandre Jamet, Catherine Juste, Ghalia Kaci, Omar Lakhdari, Severine Layec, Karine Le Roux, Emmanuelle Maguin, Pierre Renault, Nicolas Sanchez, Gaetana Vandemeulebrouck & Yohanan Winogradsky

  29. UCB Pharma SA, 28046 Madrid, Spain

    Carlos Cara

  30. Danone Research, 91120 Palaiseau, France

    Christian Chervaux, Gérard Denariaz, Johan van Hylckama-Vlieg, Jan Knol & Raish Oozeer

  31. European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany

    Konrad U. Foerstner, Wolfgang Huber, Shinichi Sunagawa & Georg Zeller

  32. Heidelberger Strasse 24, 64285 Darmstadt, Germany

    Konrad U. Foerstner

  33. Center for Biological Sequence Analysis, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark

    Carsten Friss

  34. Institute of Genetics and Molecular and Cellular Biology, CNRS, INSERM, University of Strasbourg, 67404 Illkrich, France

    Jean Muller

  35. The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK

    Julian Parkhill & Keith Turner

  36. Istituto Europeo di Oncologia, 20100 Milan, Italy

    Maria Rescigno

  37. Institut Mérieux, 17 rue Burgelat, 69002 Lyon, France

    Christian Brechot, Alexandre Mérieux & Christine M'rini

  38. Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, DK-2200 Copenhagen, Denmark.,

    Karsten Kristiansen

Authors
  1. Manimozhiyan Arumugam
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  2. Jeroen Raes
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  3. Eric Pelletier
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  4. Denis Le Paslier
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  5. Takuji Yamada
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  6. Daniel R. Mende
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  7. Gabriel R. Fernandes
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  8. Julien Tap
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  9. Thomas Bruls
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  10. Jean-Michel Batto
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  14. Leyden Fernandez
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  42. Peer Bork
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Consortia

MetaHIT Consortium (additional members)

  • María Antolín
  • , François Artiguenave
  • , Hervé M. Blottiere
  • , Mathieu Almeida
  • , Christian Brechot
  • , Carlos Cara
  • , Christian Chervaux
  • , Antonella Cultrone
  • , Christine Delorme
  • , Gérard Denariaz
  • , Rozenn Dervyn
  • , Konrad U. Foerstner
  • , Carsten Friss
  • , Maarten van de Guchte
  • , Eric Guedon
  • , Florence Haimet
  • , Wolfgang Huber
  • , Johan van Hylckama-Vlieg
  • , Alexandre Jamet
  • , Catherine Juste
  • , Ghalia Kaci
  • , Jan Knol
  • , Karsten Kristiansen
  • , Omar Lakhdari
  • , Severine Layec
  • , Karine Le Roux
  • , Emmanuelle Maguin
  • , Alexandre Mérieux
  • , Raquel Melo Minardi
  • , Christine M'rini
  • , Jean Muller
  • , Raish Oozeer
  • , Julian Parkhill
  • , Pierre Renault
  • , Maria Rescigno
  • , Nicolas Sanchez
  • , Shinichi Sunagawa
  • , Antonio Torrejon
  • , Keith Turner
  • , Gaetana Vandemeulebrouck
  • , Encarna Varela
  • , Yohanan Winogradsky
  •  & Georg Zeller

Contributions

All authors are members of the Metagenomics of the Human Intestinal Tract (MetaHIT) Consortium. Jun W., F.G., O.P., W.M.d.V., S.B., J.D., Jean W., S.D.E. and P.B. managed the project. N.B., F.C., T.H., C.M. and T. N. performed clinical analyses. M.L. and F.L. performed DNA extraction. E.P., D.L.P., T.B., J.P. and E.U. performed DNA sequencing. M.A., J.R., S.D.E. and P.B. designed the analyses. M.A., J.R., T.Y., D.R.M., G.R.F., J.T., J.-M.B., M.B., L.F., L.G., M.K., H.B.N., N.P., J.Q., T.S.-P., S.T., D.T., E.G.Z., S.D.E. and P.B. performed the analyses. M.A., J.R., P.B. and S.D.E. wrote the manuscript. M.H., T.H., K.K. and the MetaHIT Consortium members contributed to the design and execution of the study.

Corresponding authors

Correspondence to S. Dusko Ehrlich or Peer Bork.

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Competing interests

The authors declare no competing financial interests.

Additional information

Raw Sanger read data from the European faecal metagenomes have been deposited in the NCBI Trace Archive with the following project identifiers: MH6 (33049), MH13 (33053), MH12 (33055), MH30 (33057), CD1 (33059), CD2 (33061), UC4 (33113), UC6 (33063), NO1 (33305), NO3 (33307), NO4 (33309), NO8 (33311), OB2 (33313), OB1 (38231), OB6 (38233), OB8 (45929), A (63073), B (63075), C (63077), D (63079), E (63081), G (63083). Contigs, genes and annotations are available to download from http://www.bork.embl.de/Docu/Arumugam_et_al_2011/.

Supplementary information

Supplementary Information

The file contains Supplementary Methods, Supplementary Notes and Supplementary References. A minor error in Supplementary Information section 2.2 was corrected on 02 June 2011. (PDF 769 kb)

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Arumugam, M., Raes, J., Pelletier, E. et al. Enterotypes of the human gut microbiome. Nature 473, 174–180 (2011). https://doi.org/10.1038/nature09944

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