Mapping the gut microecological multi-omics signatures to serum metabolome and their impact on cardiometabolic health in elderly adults

EBioMedicine. 2024 Jul:105:105209. doi: 10.1016/j.ebiom.2024.105209. Epub 2024 Jun 21.

Abstract

Background: Mapping gut microecological features to serum metabolites (SMs) will help identify functional links between gut microbiome and cardiometabolic health.

Methods: This study encompassed 836-1021 adults over 9.7 year in a cohort, assessing metabolic syndrome (MS), carotid atherosclerotic plaque (CAP), and other metadata triennially. We analyzed mid-term microbial metagenomics, targeted fecal and serum metabolomics, host genetics, and serum proteomics.

Findings: Gut microbiota and metabolites (GMM) accounted for 15.1% overall variance in 168 SMs, with individual GMM factors explaining 5.65%-10.1%, host genetics 3.23%, and sociodemographic factors 5.95%. Specifically, GMM elucidated 5.5%-49.6% variance in the top 32 GMM-explained SMs. Each 20% increase in the 32 metabolite score (derived from the 32 SMs) correlated with 73% (95% confidence interval [CI]: 53%-95%) and 19% (95% CI: 11%-27%) increases in MS and CAP incidences, respectively. Among the 32 GMM-explained SMs, sebacic acid, indoleacetic acid, and eicosapentaenoic acid were linked to MS or CAP incidence. Serum proteomics revealed certain proteins, particularly the apolipoprotein family, mediated the relationship between GMM-SMs and cardiometabolic risks.

Interpretation: This study reveals the significant influence of GMM on SM profiles and illustrates the intricate connections between GMM-explained SMs, serum proteins, and the incidence of MS and CAP, providing insights into the roles of gut dysbiosis in cardiometabolic health via regulating blood metabolites.

Funding: This study was jointly supported by the National Natural Science Foundation of China, Key Research and Development Program of Guangzhou, 5010 Program for Clinical Research of Sun Yat-sen University, and the 'Pioneer' and 'Leading goose' R&D Program of Zhejiang.

Keywords: Cardiometabolic health; Gut microbiota; Metabolomics; Multi-omics; Proteomics.

MeSH terms

  • Aged
  • Biomarkers / blood
  • Feces / microbiology
  • Female
  • Gastrointestinal Microbiome*
  • Humans
  • Male
  • Metabolic Syndrome* / blood
  • Metabolic Syndrome* / epidemiology
  • Metabolome*
  • Metabolomics* / methods
  • Metagenomics / methods
  • Middle Aged
  • Multiomics
  • Proteomics / methods

Substances

  • Biomarkers