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Associations between untargeted plasma metabolomic signatures and gut microbiota composition in the Milieu Intérieur population of healthy adults

Published online by Cambridge University Press:  10 December 2020

Valentin Partula
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France University of Paris-VII Denis Diderot, Université de Paris, 75000 Paris, France
Mélanie Deschasaux-Tanguy
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France
Stanislas Mondot
Affiliation:
PhylHom Team, MICALIS Institute (Inrae/AgroParisTech), 78350 Jouy-en-Josas, France
Agnès Victor-Bala
Affiliation:
Chemistry, Structure, and Properties of Biomaterials and Therapeutic Agents CSPBAT, Nanomedicine, Biomarkers and Detection Team (CNRS U7244/Université Sorbonne Paris Nord), 93000 Bobigny, France
Nadia Bouchemal
Affiliation:
Chemistry, Structure, and Properties of Biomaterials and Therapeutic Agents CSPBAT, Nanomedicine, Biomarkers and Detection Team (CNRS U7244/Université Sorbonne Paris Nord), 93000 Bobigny, France
Lucie Lécuyer
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France
Christine Bobin-Dubigeon
Affiliation:
Department of Biopathology, Institut de Cancérologie de l’Ouest, 44800 Saint-Herblain, France Sea, Molecules, Health MMS EA2160 (CNRS FR3473/Université de Nantes), 44000 Nantes, France
Marion J. Torres
Affiliation:
Nutritional Surveillance and Epidemiology Team (ESEN), French Public Health Agency, Sorbonne Paris Nord University, Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France
Emmanuelle Kesse-Guyot
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France
Bruno Charbit
Affiliation:
Centre for Translational Research, Institut Pasteur, 75000 Paris, France
Etienne Patin
Affiliation:
Human Evolutionary Genetics Laboratory (CNRS URA3012/Institut Pasteur), 75000 Paris, France
Karen E. Assmann
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France
Paule Latino-Martel
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France
Chantal Julia
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France Department of Public Health, AP-HP Paris Seine-Saint-Denis University Hospital System, 93000 Bobigny, France
Pilar Galan
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France
Serge Hercberg
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France Department of Public Health, AP-HP Paris Seine-Saint-Denis University Hospital System, 93000 Bobigny, France
Lluis Quintana-Murci
Affiliation:
Human Evolutionary Genetics Laboratory (CNRS URA3012/Institut Pasteur), 75000 Paris, France
Matthew L. Albert
Affiliation:
Department of Immunology and Infectious Diseases, Insitro, San Fransisco, CA 94080, USA
Darragh Duffy
Affiliation:
Immunobiology of Dendritic Cells Laboratory (Inserm U1223/Institut Pasteur), 75000 Paris, France
Olivier Lantz
Affiliation:
Curie Institute, PSL University, Inserm U932, 75000 Paris, France Clinical Investigation Center CIC-BT1428 (Institut Gustave Roussy/Institut Curie), Inserm, 75000 Paris, France
Philippe Savarin
Affiliation:
Chemistry, Structure, and Properties of Biomaterials and Therapeutic Agents CSPBAT, Nanomedicine, Biomarkers and Detection Team (CNRS U7244/Université Sorbonne Paris Nord), 93000 Bobigny, France
Mohamed Nawfal Triba
Affiliation:
Chemistry, Structure, and Properties of Biomaterials and Therapeutic Agents CSPBAT, Nanomedicine, Biomarkers and Detection Team (CNRS U7244/Université Sorbonne Paris Nord), 93000 Bobigny, France
Mathilde Touvier
Affiliation:
Sorbonne Paris Nord University, INSERM, INRAE, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center – University of Paris (CRESS), 93000 Bobigny, France
The Milieu Intérieur Consortium
Affiliation:
The Milieu Intérieur Consortium, Pasteur Institute, 75000 Paris, France
Corresponding

Abstract

Host–microbial co-metabolism products are being increasingly recognised to play important roles in physiological processes. However, studies undertaking a comprehensive approach to consider host–microbial metabolic relationships remain scarce. Metabolomic analysis yielding detailed information regarding metabolites found in a given biological compartment holds promise for such an approach. This work aimed to explore the associations between host plasma metabolomic signatures and gut microbiota composition in healthy adults of the Milieu Intérieur study. For 846 subjects, gut microbiota composition was profiled through sequencing of the 16S rRNA gene in stools. Metabolomic signatures were generated through proton NMR analysis of plasma. The associations between metabolomic variables and α- and β-diversity indexes and relative taxa abundances were tested using multi-adjusted partial Spearman correlations, permutational ANOVA and multivariate associations with linear models, respectively. A multiple testing correction was applied (Benjamini–Hochberg, 10 % false discovery rate). Microbial richness was negatively associated with lipid-related signals and positively associated with amino acids, choline, creatinine, glucose and citrate (−0·133 ≤ Spearman’s ρ ≤ 0·126). Specific associations between metabolomic signals and abundances of taxa were detected (twenty-five at the genus level and nineteen at the species level): notably, numerous associations were observed for creatinine (positively associated with eleven species and negatively associated with Faecalibacterium prausnitzii). This large-scale population-based study highlights metabolites associated with gut microbial features and provides new insights into the understanding of complex host–gut microbiota metabolic relationships. In particular, our results support the implication of a ‘gut–kidney axis’. More studies providing a detailed exploration of these complex interactions and their implications for host health are needed.

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Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Nutrition Society

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Footnotes

These authors are considered as co-first authors.

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Associations between untargeted plasma metabolomic signatures and gut microbiota composition in the Milieu Intérieur population of healthy adults
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