Genome scale metabolic network modelling for metabolic profile predictions

PLoS Comput Biol. 2024 Feb 22;20(2):e1011381. doi: 10.1371/journal.pcbi.1011381. eCollection 2024 Feb.

Abstract

Metabolic profiling (metabolomics) aims at measuring small molecules (metabolites) in complex samples like blood or urine for human health studies. While biomarker-based assessment often relies on a single molecule, metabolic profiling combines several metabolites to create a more complex and more specific fingerprint of the disease. However, in contrast to genomics, there is no unique metabolomics setup able to measure the entire metabolome. This challenge leads to tedious and resource consuming preliminary studies to be able to design the right metabolomics experiment. In that context, computer assisted metabolic profiling can be of strong added value to design metabolomics studies more quickly and efficiently. We propose a constraint-based modelling approach which predicts in silico profiles of metabolites that are more likely to be differentially abundant under a given metabolic perturbation (e.g. due to a genetic disease), using flux simulation. In genome-scale metabolic networks, the fluxes of exchange reactions, also known as the flow of metabolites through their external transport reactions, can be simulated and compared between control and disease conditions in order to calculate changes in metabolite import and export. These import/export flux differences would be expected to induce changes in circulating biofluid levels of those metabolites, which can then be interpreted as potential biomarkers or metabolites of interest. In this study, we present SAMBA (SAMpling Biomarker Analysis), an approach which simulates fluxes in exchange reactions following a metabolic perturbation using random sampling, compares the simulated flux distributions between the baseline and modulated conditions, and ranks predicted differentially exchanged metabolites as potential biomarkers for the perturbation. We show that there is a good fit between simulated metabolic exchange profiles and experimental differential metabolites detected in plasma, such as patient data from the disease database OMIM, and metabolic trait-SNP associations found in mGWAS studies. These biomarker recommendations can provide insight into the underlying mechanism or metabolic pathway perturbation lying behind observed metabolite differential abundances, and suggest new metabolites as potential avenues for further experimental analyses.

MeSH terms

  • Biomarkers
  • Genome
  • Humans
  • Metabolic Networks and Pathways
  • Metabolome* / genetics
  • Metabolomics*

Substances

  • Biomarkers

Grants and funding

JC is supported by a state-funded PhD contract (Ministère de l’Enseignement supérieur, de la Recherche et de l’Innovation, Grant 2020-2), and by MetaboHUB (Grant 11-INBS-0010). FJ is supported by the Agence Nationale de la Recherche (ANR) through MetaboHUB (Grant ANR-INBS-0010), as well as the MetClassNet project (ANR-19-CE45-0021 and Deutsche Forschungsgemeinschaft DFG: 431572533). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.