Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity

Alexandra Zhernakova; Alexander Kurilshikov; Marc Jan Bonder; Ettje F. Tigchelaar; Melanie Schirmer; Tommi Vatanen; Zlatan Mujagic; Arnau Vich Vila; Gwen Falony; Sara Vieira-Silva; Jun Wang; Floris Imhann; Eelke Brandsma; Soesma A. Jankipersadsing; Marie Joossens; Maria Carmen Cenit; Patrick Deelen; Morris A. Swertz; LifeLines cohort study; Rinse K. Weersma; Edith J. M. Feskens; Mihai G. Netea; Dirk Gevers; Daisy Jonkers; Lude Franke; Yurii S. Aulchenko; Curtis Huttenhower; Jeroen Raes; Marten H. Hofker; Ramnik J. Xavier; Cisca Wijmenga; Jingyuan Fu

doi:10.1126/science.aad3369

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Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity

Alexandra Zhernakova¹,²,*,
Alexander Kurilshikov³,⁴,^†,
Marc Jan Bonder¹,^†,
Ettje F. Tigchelaar¹,²,^†,
Melanie Schirmer⁵,⁶,
Tommi Vatanen⁵,⁷,
Zlatan Mujagic²,⁸,
Arnau Vich Vila⁹,
Gwen Falony¹⁰,¹¹,
Sara Vieira-Silva¹⁰,¹¹,
Jun Wang¹⁰,¹¹,
Floris Imhann⁹,
Eelke Brandsma¹²,
Soesma A. Jankipersadsing¹,
Marie Joossens¹⁰,¹¹,¹³,
Maria Carmen Cenit¹,¹⁴,¹⁵,
Patrick Deelen¹,¹⁶,
Morris A. Swertz¹,¹⁶,
LifeLines cohort study,
Rinse K. Weersma⁹,
Edith J. M. Feskens²,¹⁷,
Mihai G. Netea¹⁸,
Dirk Gevers⁵,‡,
Daisy Jonkers⁸,
Lude Franke¹,
Yurii S. Aulchenko⁴,¹⁹,²⁰,²¹,
Curtis Huttenhower⁵,⁶,
Jeroen Raes¹⁰,¹¹,¹³,
Marten H. Hofker¹²,
Ramnik J. Xavier⁵,²²,²³,²⁴,
Cisca Wijmenga¹,*,^§,
Jingyuan Fu¹,¹²,*,^§

¹University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.
²Top Institute Food and Nutrition, Wageningen, Netherlands.
³Institute of Chemical Biology and Fundamental Medicine SB RAS, Novosibirsk, Russia.
⁴Novosibirsk State University, Novosibirsk, Russia.
⁵The Broad Institute of MIT and Harvard, Cambridge, MA, USA.
⁶Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA.
⁷Department of Computer Science, Aalto University School of Science, Espoo, Finland.
⁸Division of Gastroenterology-Hepatology, Department of Internal Medicine, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, Maastricht, Netherlands.
⁹University of Groningen, University Medical Center Groningen, Department of Gastroenterology and Hepatology, Groningen, Netherlands.
¹⁰KU Leuven–University of Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Molecular Bacteriology, Leuven, Belgium.
¹¹VIB, Center for the Biology of Disease, Leuven, Belgium.
¹²University of Groningen, University Medical Center Groningen, Department of Pediatrics, Groningen, Netherlands.
¹³Vrije Universiteit Brussel, Faculty of Sciences and Bioengineering Sciences, Microbiology Unit, Brussels, Belgium.
¹⁴Microbial Ecology, Nutrition and Health Research Group, Institute of Agrochemistry and Food Technology, National Research Council (IATA-CSIC), Valencia, Spain.
¹⁵Department of Pediatrics, Dr. Peset University Hospital, Valencia, Spain.
¹⁶University of Groningen, University Medical Center Groningen, Genomics Coordination Center, Groningen, Netherlands.
¹⁷Division of Human Nutrition, Wageningen University, Wageningen, Netherlands.
¹⁸Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, Netherlands.
¹⁹Centre for Global Health Research, Usher Institute of Population Health Sciences and Informatics, University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, UK.
²⁰PolyOmica, Groningen, Netherlands.
²¹Institute of Cytology and Genetics SB RAS, Novosibirsk, Russia.
²²Center for Computational and Integrative Biology, Massachusetts General Hospital, Boston, MA, USA.
²³Gastrointestinal Unit and Center for the Study of Inflammatory Bowel Disease, Massachusetts General Hospital, Boston, MA, USA.
²⁴Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA.

↵*Corresponding author. Email: a.zhernakova{at}umcg.nl (A.Z.); c.wijmenga{at}umcg.nl (C.W.); j.fu{at}umcg.nl (J.F.)

↵† These authors contributed equally to this work.
§ These authors contributed equally to this work.

↵‡ Present address: Janssen Human Microbiome Institute, Janssen Research and Development, Cambridge, MA, USA.

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Science 29 Apr 2016:
Vol. 352, Issue 6285, pp. 565-569
DOI: 10.1126/science.aad3369

Alexandra Zhernakova

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

2Top Institute Food and Nutrition, Wageningen, Netherlands.

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For correspondence: a.zhernakova@umcg.nl c.wijmenga@umcg.nl j.fu@umcg.nl

Alexander Kurilshikov

3Institute of Chemical Biology and Fundamental Medicine SB RAS, Novosibirsk, Russia.

4Novosibirsk State University, Novosibirsk, Russia.

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Marc Jan Bonder

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

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Ettje F. Tigchelaar

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

2Top Institute Food and Nutrition, Wageningen, Netherlands.

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Melanie Schirmer

5The Broad Institute of MIT and Harvard, Cambridge, MA, USA.

6Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA.

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Tommi Vatanen

5The Broad Institute of MIT and Harvard, Cambridge, MA, USA.

7Department of Computer Science, Aalto University School of Science, Espoo, Finland.

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Zlatan Mujagic

2Top Institute Food and Nutrition, Wageningen, Netherlands.

8Division of Gastroenterology-Hepatology, Department of Internal Medicine, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University Medical Center, Maastricht, Netherlands.

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Arnau Vich Vila

9University of Groningen, University Medical Center Groningen, Department of Gastroenterology and Hepatology, Groningen, Netherlands.

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Gwen Falony

10KU Leuven–University of Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Molecular Bacteriology, Leuven, Belgium.

11VIB, Center for the Biology of Disease, Leuven, Belgium.

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Sara Vieira-Silva

10KU Leuven–University of Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Molecular Bacteriology, Leuven, Belgium.

11VIB, Center for the Biology of Disease, Leuven, Belgium.

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Jun Wang

10KU Leuven–University of Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Molecular Bacteriology, Leuven, Belgium.

11VIB, Center for the Biology of Disease, Leuven, Belgium.

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Floris Imhann

9University of Groningen, University Medical Center Groningen, Department of Gastroenterology and Hepatology, Groningen, Netherlands.

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Eelke Brandsma

12University of Groningen, University Medical Center Groningen, Department of Pediatrics, Groningen, Netherlands.

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Soesma A. Jankipersadsing

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

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Marie Joossens

10KU Leuven–University of Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Molecular Bacteriology, Leuven, Belgium.

11VIB, Center for the Biology of Disease, Leuven, Belgium.

13Vrije Universiteit Brussel, Faculty of Sciences and Bioengineering Sciences, Microbiology Unit, Brussels, Belgium.

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Maria Carmen Cenit

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

14Microbial Ecology, Nutrition and Health Research Group, Institute of Agrochemistry and Food Technology, National Research Council (IATA-CSIC), Valencia, Spain.

15Department of Pediatrics, Dr. Peset University Hospital, Valencia, Spain.

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Patrick Deelen

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

16University of Groningen, University Medical Center Groningen, Genomics Coordination Center, Groningen, Netherlands.

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Morris A. Swertz

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

16University of Groningen, University Medical Center Groningen, Genomics Coordination Center, Groningen, Netherlands.

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Rinse K. Weersma

9University of Groningen, University Medical Center Groningen, Department of Gastroenterology and Hepatology, Groningen, Netherlands.

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Edith J. M. Feskens

2Top Institute Food and Nutrition, Wageningen, Netherlands.

17Division of Human Nutrition, Wageningen University, Wageningen, Netherlands.

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Mihai G. Netea

18Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, Netherlands.

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Dirk Gevers

5The Broad Institute of MIT and Harvard, Cambridge, MA, USA.

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Daisy Jonkers

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Lude Franke

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

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Yurii S. Aulchenko

4Novosibirsk State University, Novosibirsk, Russia.

19Centre for Global Health Research, Usher Institute of Population Health Sciences and Informatics, University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, UK.

20PolyOmica, Groningen, Netherlands.

21Institute of Cytology and Genetics SB RAS, Novosibirsk, Russia.

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Curtis Huttenhower

5The Broad Institute of MIT and Harvard, Cambridge, MA, USA.

6Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA.

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Jeroen Raes

10KU Leuven–University of Leuven, Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Molecular Bacteriology, Leuven, Belgium.

11VIB, Center for the Biology of Disease, Leuven, Belgium.

13Vrije Universiteit Brussel, Faculty of Sciences and Bioengineering Sciences, Microbiology Unit, Brussels, Belgium.

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Marten H. Hofker

12University of Groningen, University Medical Center Groningen, Department of Pediatrics, Groningen, Netherlands.

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Ramnik J. Xavier

5The Broad Institute of MIT and Harvard, Cambridge, MA, USA.

22Center for Computational and Integrative Biology, Massachusetts General Hospital, Boston, MA, USA.

23Gastrointestinal Unit and Center for the Study of Inflammatory Bowel Disease, Massachusetts General Hospital, Boston, MA, USA.

24Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA.

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Cisca Wijmenga

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

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For correspondence: a.zhernakova@umcg.nl c.wijmenga@umcg.nl j.fu@umcg.nl

Jingyuan Fu

1University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, Netherlands.

12University of Groningen, University Medical Center Groningen, Department of Pediatrics, Groningen, Netherlands.

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For correspondence: a.zhernakova@umcg.nl c.wijmenga@umcg.nl j.fu@umcg.nl

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