Influence of the microbiome, diet and genetics on inter-individual variation in the human plasma metabolome

The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual’s genetics and the composition of their diet and gut microbiome. Here, by assessing 1,183 plasma metabolites in 1,368 extensively phenotyped individuals from the Lifelines DEEP and Geno...

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Published in:Nature medicine Vol. 28; no. 11; pp. 2333 - 2343
Main Authors: Chen, Lianmin, Zhernakova, Daria V., Kurilshikov, Alexander, Andreu-Sánchez, Sergio, Wang, Daoming, Augustijn, Hannah E., Vich Vila, Arnau, Weersma, Rinse K., Medema, Marnix H., Netea, Mihai G., Kuipers, Folkert, Wijmenga, Cisca, Zhernakova, Alexandra, Fu, Jingyuan
Format: Journal Article
Language:English
Published: New York Nature Publishing Group US 01.11.2022
Nature Publishing Group
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ISSN:1078-8956, 1546-170X, 1546-170X
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Abstract The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual’s genetics and the composition of their diet and gut microbiome. Here, by assessing 1,183 plasma metabolites in 1,368 extensively phenotyped individuals from the Lifelines DEEP and Genome of the Netherlands cohorts, we quantified the proportion of inter-individual variation in the plasma metabolome explained by different factors, characterizing 610, 85 and 38 metabolites as dominantly associated with diet, the gut microbiome and genetics, respectively. Moreover, a diet quality score derived from metabolite levels was significantly associated with diet quality, as assessed by a detailed food frequency questionnaire. Through Mendelian randomization and mediation analyses, we revealed putative causal relationships between diet, the gut microbiome and metabolites. For example, Mendelian randomization analyses support a potential causal effect of Eubacterium rectale in decreasing plasma levels of hydrogen sulfite—a toxin that affects cardiovascular function. Lastly, based on analysis of the plasma metabolome of 311 individuals at two time points separated by 4 years, we observed a positive correlation between the stability of metabolite levels and the amount of variance in the levels of that metabolite that could be explained in our analysis. Altogether, characterization of factors that explain inter-individual variation in the plasma metabolome can help design approaches for modulating diet or the gut microbiome to shape a healthy metabolome. The influence of an individual’s genetics, diet and gut microbiome on their plasma metabolome was studied in 1,368 individuals and Mendelian randomization and mediation analyses were used to unveil causal relationships between diet, the gut microbiome and the metabolome.
AbstractList The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual’s genetics and the composition of their diet and gut microbiome. Here, by assessing 1,183 plasma metabolites in 1,368 extensively phenotyped individuals from the Lifelines DEEP and Genome of the Netherlands cohorts, we quantified the proportion of inter-individual variation in the plasma metabolome explained by different factors, characterizing 610, 85 and 38 metabolites as dominantly associated with diet, the gut microbiome and genetics, respectively. Moreover, a diet quality score derived from metabolite levels was significantly associated with diet quality, as assessed by a detailed food frequency questionnaire. Through Mendelian randomization and mediation analyses, we revealed putative causal relationships between diet, the gut microbiome and metabolites. For example, Mendelian randomization analyses support a potential causal effect of Eubacterium rectale in decreasing plasma levels of hydrogen sulfite—a toxin that affects cardiovascular function. Lastly, based on analysis of the plasma metabolome of 311 individuals at two time points separated by 4 years, we observed a positive correlation between the stability of metabolite levels and the amount of variance in the levels of that metabolite that could be explained in our analysis. Altogether, characterization of factors that explain inter-individual variation in the plasma metabolome can help design approaches for modulating diet or the gut microbiome to shape a healthy metabolome. The influence of an individual’s genetics, diet and gut microbiome on their plasma metabolome was studied in 1,368 individuals and Mendelian randomization and mediation analyses were used to unveil causal relationships between diet, the gut microbiome and the metabolome.
The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual’s genetics and the composition of their diet and gut microbiome. Here, by assessing 1,183 plasma metabolites in 1,368 extensively phenotyped individuals from the Lifelines DEEP and Genome of the Netherlands cohorts, we quantified the proportion of inter-individual variation in the plasma metabolome explained by different factors, characterizing 610, 85 and 38 metabolites as dominantly associated with diet, the gut microbiome and genetics, respectively. Moreover, a diet quality score derived from metabolite levels was significantly associated with diet quality, as assessed by a detailed food frequency questionnaire. Through Mendelian randomization and mediation analyses, we revealed putative causal relationships between diet, the gut microbiome and metabolites. For example, Mendelian randomization analyses support a potential causal effect of Eubacterium rectale in decreasing plasma levels of hydrogen sulfite—a toxin that affects cardiovascular function. Lastly, based on analysis of the plasma metabolome of 311 individuals at two time points separated by 4 years, we observed a positive correlation between the stability of metabolite levels and the amount of variance in the levels of that metabolite that could be explained in our analysis. Altogether, characterization of factors that explain inter-individual variation in the plasma metabolome can help design approaches for modulating diet or the gut microbiome to shape a healthy metabolome.
The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual's genetics and the composition of their diet and gut microbiome. Here, by assessing 1,183 plasma metabolites in 1,368 extensively phenotyped individuals from the Lifelines DEEP and Genome of the Netherlands cohorts, we quantified the proportion of inter-individual variation in the plasma metabolome explained by different factors, characterizing 610, 85 and 38 metabolites as dominantly associated with diet, the gut microbiome and genetics, respectively. Moreover, a diet quality score derived from metabolite levels was significantly associated with diet quality, as assessed by a detailed food frequency questionnaire. Through Mendelian randomization and mediation analyses, we revealed putative causal relationships between diet, the gut microbiome and metabolites. For example, Mendelian randomization analyses support a potential causal effect of Eubacterium rectale in decreasing plasma levels of hydrogen sulfite-a toxin that affects cardiovascular function. Lastly, based on analysis of the plasma metabolome of 311 individuals at two time points separated by 4 years, we observed a positive correlation between the stability of metabolite levels and the amount of variance in the levels of that metabolite that could be explained in our analysis. Altogether, characterization of factors that explain inter-individual variation in the plasma metabolome can help design approaches for modulating diet or the gut microbiome to shape a healthy metabolome.The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual's genetics and the composition of their diet and gut microbiome. Here, by assessing 1,183 plasma metabolites in 1,368 extensively phenotyped individuals from the Lifelines DEEP and Genome of the Netherlands cohorts, we quantified the proportion of inter-individual variation in the plasma metabolome explained by different factors, characterizing 610, 85 and 38 metabolites as dominantly associated with diet, the gut microbiome and genetics, respectively. Moreover, a diet quality score derived from metabolite levels was significantly associated with diet quality, as assessed by a detailed food frequency questionnaire. Through Mendelian randomization and mediation analyses, we revealed putative causal relationships between diet, the gut microbiome and metabolites. For example, Mendelian randomization analyses support a potential causal effect of Eubacterium rectale in decreasing plasma levels of hydrogen sulfite-a toxin that affects cardiovascular function. Lastly, based on analysis of the plasma metabolome of 311 individuals at two time points separated by 4 years, we observed a positive correlation between the stability of metabolite levels and the amount of variance in the levels of that metabolite that could be explained in our analysis. Altogether, characterization of factors that explain inter-individual variation in the plasma metabolome can help design approaches for modulating diet or the gut microbiome to shape a healthy metabolome.
The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual's genetics and the composition of their diet and gut microbiome. Here, by assessing 1,183 plasma metabolites in 1,368 extensively phenotyped individuals from the Lifelines DEEP and Genome of the Netherlands cohorts, we quantified the proportion of inter-individual variation in the plasma metabolome explained by different factors, characterizing 610, 85 and 38 metabolites as dominantly associated with diet, the gut microbiome and genetics, respectively. Moreover, a diet quality score derived from metabolite levels was significantly associated with diet quality, as assessed by a detailed food frequency questionnaire. Through Mendelian randomization and mediation analyses, we revealed putative causal relationships between diet, the gut microbiome and metabolites. For example, Mendelian randomization analyses support a potential causal effect of Eubacterium rectale in decreasing plasma levels of hydrogen sulfite-a toxin that affects cardiovascular function. Lastly, based on analysis of the plasma metabolome of 311 individuals at two time points separated by 4 years, we observed a positive correlation between the stability of metabolite levels and the amount of variance in the levels of that metabolite that could be explained in our analysis. Altogether, characterization of factors that explain inter-individual variation in the plasma metabolome can help design approaches for modulating diet or the gut microbiome to shape a healthy metabolome.
The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual’s genetics and the composition of their diet and gut microbiome. Here, by assessing 1,183 plasma metabolites in 1,368 extensively phenotyped individuals from the Lifelines DEEP and Genome of the Netherlands cohorts, we quantified the proportion of inter-individual variation in the plasma metabolome explained by different factors, characterizing 610, 85 and 38 metabolites as dominantly associated with diet, the gut microbiome and genetics, respectively. Moreover, a diet quality score derived from metabolite levels was significantly associated with diet quality, as assessed by a detailed food frequency questionnaire. Through Mendelian randomization and mediation analyses, we revealed putative causal relationships between diet, the gut microbiome and metabolites. For example, Mendelian randomization analyses support a potential causal effect of Eubacterium rectale in decreasing plasma levels of hydrogen sulfite—a toxin that affects cardiovascular function. Lastly, based on analysis of the plasma metabolome of 311 individuals at two time points separated by 4 years, we observed a positive correlation between the stability of metabolite levels and the amount of variance in the levels of that metabolite that could be explained in our analysis. Altogether, characterization of factors that explain inter-individual variation in the plasma metabolome can help design approaches for modulating diet or the gut microbiome to shape a healthy metabolome. The influence of an individual’s genetics, diet and gut microbiome on their plasma metabolome was studied in 1,368 individuals and Mendelian randomization and mediation analyses were used to unveil causal relationships between diet, the gut microbiome and the metabolome.
Author Wijmenga, Cisca
Fu, Jingyuan
Kurilshikov, Alexander
Vich Vila, Arnau
Augustijn, Hannah E.
Weersma, Rinse K.
Netea, Mihai G.
Kuipers, Folkert
Medema, Marnix H.
Andreu-Sánchez, Sergio
Zhernakova, Daria V.
Zhernakova, Alexandra
Chen, Lianmin
Wang, Daoming
Author_xml – sequence: 1
  givenname: Lianmin
  orcidid: 0000-0003-0660-3518
  surname: Chen
  fullname: Chen, Lianmin
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen, Department of Pediatrics, University of Groningen, University Medical Center Groningen, Department of Cardiology, Nanjing Medical University, The First Affiliated Hospital of Nanjing Medical University, Cardiovascular Research Center, The Affiliated Suzhou Hospital of Nanjing Medical University, Suzhou Municipal Hospital, Gusu School, Nanjing Medical University
– sequence: 2
  givenname: Daria V.
  orcidid: 0000-0001-6531-3890
  surname: Zhernakova
  fullname: Zhernakova, Daria V.
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen, Laboratory of Genomic Diversity, Center for Computer Technologies, ITMO University
– sequence: 3
  givenname: Alexander
  orcidid: 0000-0003-2541-5627
  surname: Kurilshikov
  fullname: Kurilshikov, Alexander
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen
– sequence: 4
  givenname: Sergio
  orcidid: 0000-0002-3503-9971
  surname: Andreu-Sánchez
  fullname: Andreu-Sánchez, Sergio
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen, Department of Pediatrics, University of Groningen, University Medical Center Groningen
– sequence: 5
  givenname: Daoming
  orcidid: 0000-0003-4623-8527
  surname: Wang
  fullname: Wang, Daoming
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen
– sequence: 6
  givenname: Hannah E.
  surname: Augustijn
  fullname: Augustijn, Hannah E.
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen, Bioinformatics Group, Wageningen University
– sequence: 7
  givenname: Arnau
  orcidid: 0000-0003-4691-5583
  surname: Vich Vila
  fullname: Vich Vila, Arnau
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen, Department of Gastroenterology and Hepatology, University of Groningen, University Medical Center Groningen
– sequence: 9
  givenname: Rinse K.
  surname: Weersma
  fullname: Weersma, Rinse K.
  organization: Department of Gastroenterology and Hepatology, University of Groningen, University Medical Center Groningen
– sequence: 10
  givenname: Marnix H.
  orcidid: 0000-0002-2191-2821
  surname: Medema
  fullname: Medema, Marnix H.
  organization: Bioinformatics Group, Wageningen University
– sequence: 11
  givenname: Mihai G.
  orcidid: 0000-0003-2421-6052
  surname: Netea
  fullname: Netea, Mihai G.
  organization: Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Department of Immunology and Metabolism, Life and Medical Sciences Institute, University of Bonn
– sequence: 12
  givenname: Folkert
  orcidid: 0000-0003-2518-737X
  surname: Kuipers
  fullname: Kuipers, Folkert
  organization: Department of Pediatrics, University of Groningen, University Medical Center Groningen, European Research Institute for the Biology of Ageing, University of Groningen, University Medical Center Groningen
– sequence: 13
  givenname: Cisca
  orcidid: 0000-0002-5635-1614
  surname: Wijmenga
  fullname: Wijmenga, Cisca
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen
– sequence: 14
  givenname: Alexandra
  orcidid: 0000-0002-4574-0841
  surname: Zhernakova
  fullname: Zhernakova, Alexandra
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen
– sequence: 15
  givenname: Jingyuan
  orcidid: 0000-0001-5578-1236
  surname: Fu
  fullname: Fu, Jingyuan
  email: j.fu@umcg.nl
  organization: Department of Genetics, University of Groningen, University Medical Center Groningen, Department of Pediatrics, University of Groningen, University Medical Center Groningen
BackLink https://www.ncbi.nlm.nih.gov/pubmed/36216932$$D View this record in MEDLINE/PubMed
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Snippet The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual’s genetics and the composition of their diet...
The levels of the thousands of metabolites in the human plasma metabolome are strongly influenced by an individual's genetics and the composition of their diet...
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StartPage 2333
SubjectTerms 631/208
631/208/212/2142
631/326/2565
692/308/174
Biomedical and Life Sciences
Biomedicine
Blood plasma
Cancer Research
Cardiovascular system
Diet
Feces - microbiology
Gastrointestinal Microbiome - genetics
Genetic diversity
Genetics
Genomes
Humans
Infectious Diseases
Intestinal microflora
Metabolic Diseases
Metabolites
Metabolome - genetics
Microbiomes
Microbiota - genetics
Molecular Medicine
Neurosciences
Phenotype
Plasma
Plasma levels
Quality assessment
Randomization
Sulfite
Toxins
Title Influence of the microbiome, diet and genetics on inter-individual variation in the human plasma metabolome
URI https://link.springer.com/article/10.1038/s41591-022-02014-8
https://www.ncbi.nlm.nih.gov/pubmed/36216932
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https://pubmed.ncbi.nlm.nih.gov/PMC9671809
Volume 28
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