Gut

, volume 71 , issue 12 , pages gutjnl-2021-325753

Impairment of gut microbial biotin metabolism and host biotin status in severe obesity: effect of biotin and prebiotic supplementation on improved metabolism

Eugeni Belda ^{1, 2, 3}

Lise Voland ^{1, 2}

Valentina Tremaroli ^{4, 5}

Gwen Falony ^{6, 7, 8, 9}

Solia Adriouch ^{1, 2}

Karen Elena Assmann ^{1, 2}

Edi Prifti ^{10, 11}

Judith Aron‐Wisnewsky ^{1, 2, 12, 13}

Jean Debédat ^{1, 2}

Tiphaine Le Roy ^{1, 2}

Trine Skov Nielsen ^{14, 15}

Chloé Amouyal ^{1, 2}

Sébastien André ^{1, 2}

Fabrizio Andreelli ^{1, 2}

Matthias Blüher ^{16, 17}

Rima Chakaroun ^{16, 17}

Julien Chilloux ^{18, 19}

Luis Pedro Coelho ^{20, 21, 22}

Maria Dao ^{1, 2}

Promi Das ^{23, 24}

Soraya Fellahi ^{2, 25, 26, 27}

Sofia K. Forslund ^{28, 29}

N. Galleron ^{30, 31}

Thomas Blom Hansen ^{14, 15}

Bridget Holmes ^{32, 33}

Boyang Ji ^{23, 24}

Helle Krogh Pedersen ^{14, 15}

Phuong Le ^{1, 2}

Emmanuelle Le Chatelier ^{30, 31}

Christian Lewinter ^{34, 35}

Louise Mannerås-Holm ^{4, 5}

Florian Marquet ^{1, 2}

Myridakis Antonis ^{36, 37}

Veronique Pelloux ^{1, 2}

Nicolas Pons ^{30, 31}

Benoit Quinquis ^{30, 31}

Christine Rouault ^{1, 2}

Hugo Roume ^{30, 31}

Joe-Elie Salem ^{38, 39}

Nataliya Sokolovska ^{1, 2}

Nadja B Søndertoft ^{14, 15}

Sothea Touch ^{1, 2}

Sara Vieira Silva ^{6, 7, 8, 9}

P Galan ^{40, 41}

J. Holst ^{14, 15}

Jens Peter Gøtze ^{35, 42}

Lars Køber ^{34, 35}

Henrik Vestergaard ^{14, 15, 43, 44}

Torben Hansen ^{14, 15, 45, 46}

Serge Hercberg ^{40, 41}

JEAN-MICHEL OPPERT ^{12, 13}

Jens Ulrik Nielsen ^{23, 24}

Ivica Letunic ^{47, 48}

M. Dumas ^{37, 49, 50}

Michael Stumvoll ^{51, 52}

O L Pedersen ^{14, 15}

P Bork ^{20, 21, 22}

Stanislav Dusko Ehrlich ^{30, 31, 53, 54}

Jean Daniel Zucker ^{1, 2, 10, 11}

Fredrik Bäckhed ^{4, 5}

Jeroen Raes ^{6, 7, 8, 9}

Karine Clément ^{1, 2, 12, 13}

Hide authors affiliations Show authors affiliations: 54 affiliations

Nutrition and Obesities: Systemic Approaches, NutriOmics, Research Unit

Sorbonne Université, INSERM

Sorbonne University

French Institute of Health and Medical Research

Integrative Phenomics

⁴

Wallenberg Laboratory, Department of Molecular and Clinical Medicine, Sahlgrenska Center for Cardiovascular and Metabolic Research

⁵

university of Gothenburg |

⁶

Center for Microbiology

⁷

VIB

⁸

Vlaams Instituut voor Biotechnologie |

⁹

VIB-KU LEUVEN |

¹⁰

Unité de Modélisation Mathématique et Informatique des Systèmes Complexes, UMMISCO

¹¹

Sorbonne Université, IRD |

¹²

Department of Nutrition, Pitié-Salpêtrière Hospital

¹³

Assistance Publique - Hopitaux de Paris

¹⁴

Center for Basic Metabolic Research

¹⁵

Novo Nordisk Foundation, University of Copenhagen

University of Copenhagen

Novo Nordisk

¹⁶

Medical Department III - Endocrinology, Nephrology, Rheumatology - Medical Center, Faculty of Medicine

¹⁷

University of Leipzig |

¹⁸

Division of Systems Medicine, Department of Metabolism, Digestion and Reproduction

¹⁹

Imperial College London Faculty of Medicine |

²⁰

Structural and Computational Biology

²¹

EUROPEAN MOLECULAR BIOLOGY LABORATORY |

²²

MOLECULAR MEDICINE PARTNERSHIP UNIT

²³

Department of Biology

²⁴

Chalmers University of Technology |

²⁵

Functional Unit, Biochemistry and Hormonology Department

²⁶

enon Hospital, Assistance Publique-Hôpitaux de Paris

²⁷

Saint-Antoine Research Center

²⁸

Max Delbrück Center for Molecular Medicine

²⁹

MDC

³⁰

Metagenopolis |

³¹

Université Paris-Saclay, INRAE |

³²

Centre Daniel Carasso, Global Nutrition Department

³³

Danone Nutricia Research

³⁴

Department of Cardiology

³⁵

RIGSHOSPITALET

³⁶

Department of Metabolism, Digestion and Reproduction

³⁷

IMPERIAL COLLEGE LONDON |

³⁸

Department of Pharmacology and CIC-

³⁹

Assistance Publique-Hôpitaux de Paris, AP-HP, Pitié-Salpêtrière Hospital

⁴⁰

Nutritional Epidemiology Unit

⁴¹

INSERM, INRAE, CNAM, Paris University |

⁴²

Department of Clinical Biochemistry

⁴³

Steno Diabetes Center |

⁴⁴

Copenhagen |

⁴⁵

Faculty of Health Sciences

⁴⁶

UNIVERSITY OF SOUTHERN DENMARK |

⁴⁷

Biobyte Solution

⁴⁸

GmbH

⁴⁹

Department of Surgery and Cancer, Section of Computational and Systems Medicine

⁵⁰

National Heart & Lung Institute, Section of Genomic & Environmental Medicine |

⁵¹

Helmholtz Institute for Metabolic, Obesity and Vascular Research (HI-MAG) of the Helmholtz Zentrum München |

⁵²

University of Leipzig Faculty of Medicine |

⁵³

Center for Host Microbiome Interactions

⁵⁴

King's College London Dental Institute |

Publication type: Journal Article

Publication date: 2022-01-11

BMJ

Gut

scimago Q1

wos Q1

SJR: 8.874

CiteScore: 46.7

Impact factor: 25.8

ISSN: 00175749, 14683288

DOI: 10.1136/gutjnl-2021-325753

Copy DOI

PubMed ID: 35017197

Gastroenterology

Abstract

Objectives

Gut microbiota is a key component in obesity and type 2 diabetes, yet mechanisms and metabolites central to this interaction remain unclear. We examined the human gut microbiome’s functional composition in healthy metabolic state and the most severe states of obesity and type 2 diabetes within the MetaCardis cohort. We focused on the role of B vitamins and B7/B8 biotin for regulation of host metabolic state, as these vitamins influence both microbial function and host metabolism and inflammation.

Design

We performed metagenomic analyses in 1545 subjects from the MetaCardis cohorts and different murine experiments, including germ-free and antibiotic treated animals, faecal microbiota transfer, bariatric surgery and supplementation with biotin and prebiotics in mice.

Results

Severe obesity is associated with an absolute deficiency in bacterial biotin producers and transporters, whose abundances correlate with host metabolic and inflammatory phenotypes. We found suboptimal circulating biotin levels in severe obesity and altered expression of biotin-associated genes in human adipose tissue. In mice, the absence or depletion of gut microbiota by antibiotics confirmed the microbial contribution to host biotin levels. Bariatric surgery, which improves metabolism and inflammation, associates with increased bacterial biotin producers and improved host systemic biotin in humans and mice. Finally, supplementing high-fat diet-fed mice with fructo-oligosaccharides and biotin improves not only the microbiome diversity, but also the potential of bacterial production of biotin and B vitamins, while limiting weight gain and glycaemic deterioration.

Conclusion

Strategies combining biotin and prebiotic supplementation could help prevent the deterioration of metabolic states in severe obesity.

Trial registration number

NCT02059538.

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Belda E. et al. Impairment of gut microbial biotin metabolism and host biotin status in severe obesity: effect of biotin and prebiotic supplementation on improved metabolism // Gut. 2022. Vol. 71. No. 12. p. gutjnl-2021-325753.

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@article{2022_Belda,

author = {Eugeni Belda and Lise Voland and Valentina Tremaroli and Gwen Falony and Solia Adriouch and Karen Elena Assmann and Edi Prifti and Judith Aron‐Wisnewsky and Jean Debédat and Tiphaine Le Roy and Trine Skov Nielsen and Chloé Amouyal and Sébastien André and Fabrizio Andreelli and Matthias Blüher and Rima Chakaroun and Julien Chilloux and Luis Pedro Coelho and Maria Dao and Promi Das and Soraya Fellahi and Sofia K. Forslund and N. Galleron and Thomas Blom Hansen and Bridget Holmes and Boyang Ji and Helle Krogh Pedersen and Phuong Le and Emmanuelle Le Chatelier and Christian Lewinter and Louise Mannerås-Holm and Florian Marquet and Myridakis Antonis and Veronique Pelloux and Nicolas Pons and Benoit Quinquis and Christine Rouault and Hugo Roume and Joe-Elie Salem and Nataliya Sokolovska and Nadja B Søndertoft and Sothea Touch and Sara Vieira Silva and P Galan and J. Holst and Jens Peter Gøtze and Lars Køber and Henrik Vestergaard and Torben Hansen and Serge Hercberg and others},

title = {Impairment of gut microbial biotin metabolism and host biotin status in severe obesity: effect of biotin and prebiotic supplementation on improved metabolism},

journal = {Gut},

year = {2022},

volume = {71},

publisher = {BMJ},

month = {jan},

url = {https://doi.org/10.1136/gutjnl-2021-325753},

number = {12},

pages = {gutjnl--2021--325753},

doi = {10.1136/gutjnl-2021-325753}

}

MLA

Cite this

MLA Copy

Belda, Eugeni, et al. “Impairment of gut microbial biotin metabolism and host biotin status in severe obesity: effect of biotin and prebiotic supplementation on improved metabolism.” Gut, vol. 71, no. 12, Jan. 2022, pp. gutjnl-2021-325753. https://doi.org/10.1136/gutjnl-2021-325753.

Publisher

BMJ

Journal

Gut

scimago Q1

wos Q1

SJR

8.874

CiteScore

46.7

Impact factor

25.8

ISSN

00175749 (Print)

14683288 (Electronic)

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