Distinct Diet-Microbiota-Metabolism Interactions in Overweight and Obese Pregnant Women: a Metagenomics Approach

Abstract

Diet and gut microbiota are known to modulate metabolic health. Our aim was to apply a metagenomics approach to investigate whether the diet-gut microbiota-metabolism and inflammation relationships differ in pregnant overweight and obese women. This cross-sectional study was conducted in overweight (n = 234) and obese (n = 152) women during early pregnancy. Dietary quality was measured by a validated index of diet quality (IDQ). Gut microbiota taxonomic composition and species diversity were assessed by metagenomic profiling (Illumina HiSeq platform). Markers for glucose metabolism (glucose, insulin) and low-grade inflammation (high sensitivity C-reactive protein [hsCRP], glycoprotein acetylation [GlycA]) were analyzed from blood samples. Higher IDQ scores were positively associated with a higher gut microbiota species diversity (r = 0.273, P = 0.007) in obese women, but not in overweight women. Community composition (beta diversity) was associated with the GlycA level in the overweight women (P = 0.04) but not in the obese. Further analysis at the species level revealed a positive association between the abundance of species Alistipes finegoldii and the GlycA level in overweight women (logfold change = 4.74, P = 0.04). This study has been registered at ClinicalTrials.gov under registration no. NCT01922791 (https://clinicaltrials.gov/ct2/show/NCT01922791). IMPORTANCE We observed partially distinct diet-gut microbiota-metabolism and inflammation responses in overweight and obese pregnant women. In overweight women, gut microbiota community composition and the relative abundance of A. finegoldii were associated with an inflammatory status. In obese women, a higher dietary quality was related to a higher gut microbiota diversity and a healthy inflammatory status.

Keywords: diet quality; metabolism; metagenomic; microbiota diversity; obese; obesity; overweight.

FIG 1

Summary of the findings related to associations between diet quality, alpha and beta diversity, gut microbiota, and serum markers in the overweight and obese women. In overweight women, a higher gut microbiota species richness correlates with glucose metabolism and low-grade inflammatory markers, whereas dietary quality does not associate with either species richness or species diversity (Shannon index), the indices for alpha diversity. Further, there are correlations between inflammation marker and beta diversity as well as with one bacterium species Alistipes finegoldii in only overweight women. Although the species diversity of obese women seems to be linked with higher dietary quality, this is not reflected in maternal metabolism and inflammatory status. Instead, in obese women, dietary quality correlated with maternal inflammatory marker. When all women were studied together, beta diversity associated with glucose metabolism markers. In addition, borderline significant associations were observed between species diversity and markers of glucose metabolism and inflammation. Another index, species richness was significantly associated with these markers. BMI: body mass index; IDQ: index of diet quality. Black dots indicate all women, orange dots represent only the overweight pregnant women and purple dots refer to only obese pregnant women. Associations are indicated as- solid black arrow: significant (P < 0.05), solid black arrow with two crossed lines: non-significant (P ≥ 0.1) and dashed blue arrow: borderline significant (P < 0.1) (P: multiple testing corrected P-values).