Low dietary fiber intake increases Collinsella abundance in the gut microbiota of overweight and obese pregnant women

Abstract

The gut microbiota contributes to the regulation of glucose metabolism in pregnancy. Abundance of the genus Collinsella is positively correlated with circulating insulin; however, it is unclear what determines Collinsella abundance. This study aims to validate the correlation between Collinsella and insulin and to elucidate if macronutrient intake alters Collinsella abundance and gut microbiota composition. Gut microbiota profiles were assessed by 16S rRNA sequencing in 57 overweight and 73 obese pregnant women from the SPRING (Study of PRobiotics IN Gestational diabetes) trial at 16 weeks gestation and correlated with metabolic hormone levels and macronutrient intake. Gut microbiota composition in the top and bottom 10% of dietary fiber intake was evaluated through network analysis. Collinsella abundance correlated positively with circulating insulin (rho = 0.30, p = 0.0006), independent of maternal BMI, but negatively with dietary fiber intake (rho = -0.20, p = 0.025) in this cohort. Low dietary fiber intake was associated with a gut microbiota favoring lactate fermentation while high fiber intake promotes short-chain fatty acid-producing bacteria. Low dietary fiber may enable overgrowth of Collinsella and alter the overall fermentation pattern in gut microbiota. This suggests that dietary choices during pregnancy can modify the nutritional ecology of the gut microbiota, with potential deleterious effects on the metabolic and inflammatory health of the host.

Trial registration: ANZCTR 12611001208998, registered 23/11/2011.

Keywords: Collinsella; Fiber and Obesity; Insulin; Microbiota; Pregnancy.

Figure 1.

Collinsella relative abundance and maternal circulating insulin. (A) Positive correlation between genus Collinsella and insulin levels in overweight (black) and obese pregnant women (grey). (B) Collinsella abundance in overweight (black) and obese (grey) pregnant women.

Figure 2.

Connections between Collinsella relative abundance, circulating insulin and dietary fiber intake. (A) Negative correlation between dietary fiber intake and Collinsella relative abundance. (B) Comparison of genus Collinsella between women with low and high dietary fiber intake. (C) Negative correlation between dietary fiber intake and insulin levels in overweight and obese pregnant women.

Figure 3.

Differences in microbiota composition according to high and low fiber intake. (A) Network analysis based on high (n = 13) and low (n = 13) dietary fiber intake. Genera are represented as nodes. Green nodes represent genera overrepresented in the low-fiber group. Red nodes represent genera overrepresented in the high-fiber group. Color intensity explains the strength of the associations with fiber intake. (B) Principal component analysis showing the clustering of selected samples based on high (red) and low (green) fiber intake. (C) Identification of significant associations between low and high dietary fiber groups by Anosim test.

Figure 4.

Network analysis after correction of dietary fiber by total energy intake. (A) Network analysis based on high (n = 13) and low (n = 13) dietary fiber intake. Genera are represented as nodes. Green nodes represent genera overrepresented in the low-fiber group. Red nodes represent genera overrepresented in the high-fiber group. Color intensity explains the strength of the associations with fiber intake. (B) Principal component analysis showing the clustering of selected samples based on high (red) and low (green) fiber intake. (C) Identification of significant associations between low and high dietary fiber groups by Anosim test.

Figure 5.

Predictive function analysis of gut microbiota profiles of women with low or high dietary fiber intake. Pathways predicted to be upregulated in women with low fiber intake in green bars, those upregulated in women with high fiber intake in red bars.