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Pregnancy-related changes in the maternal gut microbiota are dependent upon the mother's periconceptional diet.

ABSTRACT: Shifts in the maternal gut microbiome have been implicated in metabolic adaptations to pregnancy. We investigated how pregnancy and diet interact to influence the composition of the maternal gut microbiota. Female C57BL/6 mice were fed either a control or a high fat diet for 8 weeks prior to mating. After confirmation of pregnancy, maternal weight gain and food intake were recorded. Fecal pellets were collected at 2 timepoints prior to mating (at the beginning of the experiment, and after 6 weeks of the specified diet) and at 4 timepoints during pregnancy (gestation day 0.5, 5.5, 10.5, and 15.5). The microbial composition and predicted metabolic functionality of the non-pregnant and pregnant gut was determined via sequencing of the variable 3 region of the 16S rRNA gene. Upon conception, differences in gut microbial communities were observed in both control and high fat-fed mice, including an increase in mucin-degrading bacteria. Control versus high fat-fed pregnant mice possessed the most profound changes to their maternal gut microbiota as indicated by statistically significant taxonomic differences. High fat-fed pregnant mice, when compared to control-fed animals, were found to be significantly enriched in microbes involved in metabolic pathways favoring fatty acid, ketone, vitamin, and bile synthesis. We show that pregnancy-induced changes in the female gut microbiota occur immediately at the onset of pregnancy, are vulnerable to modulation by diet, but are not dependent upon increases in maternal weight gain during pregnancy. High fat diet intake before and during pregnancy results in distinctive shifts in the pregnant gut microbiota in a gestational-age dependent manner and these shifts predict significant differences in the abundance of genes that favor lipid metabolism, glycolysis and gluconeogenic metabolic pathways over the course of pregnancy.

SUBMITTER: Gohir W

PROVIDER: S-EPMC4826136 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Pregnancy-related changes in the maternal gut microbiota are dependent upon the mother's periconceptional diet.

Gohir Wajiha W Whelan Fiona J FJ Surette Michael G MG Moore Caroline C Schertzer Jonathan D JD Sloboda Deborah M DM

Gut microbes 20150101 5

Shifts in the maternal gut microbiome have been implicated in metabolic adaptations to pregnancy. We investigated how pregnancy and diet interact to influence the composition of the maternal gut microbiota. Female C57BL/6 mice were fed either a control or a high fat diet for 8 weeks prior to mating. After confirmation of pregnancy, maternal weight gain and food intake were recorded. Fecal pellets were collected at 2 timepoints prior to mating (at the beginning of the experiment, and after 6 week ...[more]

PMID: 26322500

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Project description:Increasing evidence suggests that maternal diet during pregnancy modifies an offspring's microbiota composition and intestinal development in a long-term manner. However, the effects of maternal soluble fiber diet during pregnancy on growth traits and the developing intestine are still underexplored. Sows were allocated to either a control or 2.0% pregelatinized waxy maize starch plus guar gum (SF) dietary treatment during gestation. Growth performance, diarrhea incidence, gut microbiota composition and metabolism, and gut permeability and inflammation status of 14-day-old suckling piglets were analyzed. The maternal SF diet improved the growth rate and decreased the incidence of diarrhea in the piglets. Next-generation sequencing analysis revealed that the intestinal microbiota composition was altered by a maternal SF diet. The fecal and plasma levels of acetate and butyrate were also increased. Furthermore, a maternal SF diet reduced the levels of plasma zonulin and fecal lipocalin-2 but increased the plasma concentrations of interleukin 10 (IL-10) and transforming growth factor ? (TGF-?). Additionally, the increased relative abundances of Lactobacillus spp. in SF piglets were positively correlated with growth rate, while the decreased abundances of Bilophila spp. were positively correlated with fecal lipocalin-2 levels. Our data reveal that a maternal SF diet during pregnancy has remarkable effects on an offspring's growth traits and intestinal permeability and inflammation, perhaps by modulating the composition and metabolism of gut microbiota.IMPORTANCE Although the direct effects of dietary soluble fiber on gut microbiota have been extensively studied, the more indirect effects of maternal nutrition solely during pregnancy on the development of the offspring's intestine are until now largely unexplored. Our data show that a maternal soluble fiber diet during pregnancy is independently associated with changes in the intestinal microbiota composition and metabolism of suckling piglets. These findings have direct implications for refining dietary recommendations in pregnancy. Moreover, a maternal soluble fiber diet reduces intestinal permeability and prevents intestinal inflammation and an excessive systemic immune response of suckling piglets. Therefore, the suckling piglets' resistance to disease was enhanced, diarrhea was reduced, and weight gain was raised. Additionally, the changes in gut microbiota in response to a maternal soluble fiber diet may also be directly correlated with the offspring's growth and gut development.

Project description:BackgroundPreclinical studies have shown that maternal gut microbiota during pregnancy play a key role in prenatal immune development but the relevance of these findings to humans is unknown. The aim of this prebirth cohort study was to investigate the association between the maternal gut microbiota in pregnancy and the composition of the infant's cord and peripheral blood immune cells over the first year of life.MethodsThe Barwon Infant Study cohort (n=1074 infants) was recruited using an unselected sampling frame. Maternal fecal samples were collected at 36 weeks of pregnancy and flow cytometry was conducted on cord/peripheral blood collected at birth, 6 and 12 months of age. Among a randomly selected sub-cohort with available samples (n=293), maternal gut microbiota was characterized by sequencing the 16S rRNA V4 region. Operational taxonomic units (OTUs) were clustered based on their abundance. Associations between maternal fecal microbiota clusters and infant granulocyte, monocyte and lymphocyte subsets were explored using compositional data analysis. Partial least squares (PLS) and regression models were used to investigate the relationships/associations between environmental, maternal and infant factors, and OTU clusters.ResultsWe identified six clusters of co-occurring OTUs. The first two components in the PLS regression explained 39% and 33% of the covariance between the maternal prenatal OTU clusters and immune cell populations in offspring at birth. A cluster in which Dialister, Escherichia, and Ruminococcus were predominant was associated with a lower proportion of granulocytes (p=0.002), and higher proportions of both central naïve CD4+ T cells (CD4+/CD45RA+/CD31-) (p<0.001) and naïve regulatory T cells (Treg) (CD4+/CD45RA+/FoxP3low) (p=0.02) in cord blood. The association with central naïve CD4+ T cells persisted to 12 months of age.ConclusionThis birth cohort study provides evidence consistent with past preclinical models that the maternal gut microbiota during pregnancy plays a role in shaping the composition of innate and adaptive elements of the infant's immune system following birth.

Project description:Background: It is well established that maternal exercise during pregnancy improves metabolic outcomes associated with obesity in mothers and offspring, however, its effects on the gut microbiota of both mother and offspring, are unknown. Here, we investigated whether wheel running exercise prior to and during pregnancy and prolonged feeding of an obesogenic diet were associated with changes in the gut microbiomes of Sprague-Dawley rat dams and their offspring. Female rats were fed either chow or obesogenic diet, and half of each diet group were given access to a running wheel 10 days before mating until delivery, while others remained sedentary. 16S rRNA gene amplicon sequencing was used to assess gut microbial communities in dams and their male and female offspring around the time of weaning. Results: Statistical analyses at the operational taxonomic unit (OTU) level revealed that maternal obesogenic diet decreased gut microbial alpha diversity and altered abundances of bacterial taxa previously associated with obesity such as Bacteroides and Blautia in dams, and their offspring of both sexes. Distance based linear modeling revealed that the relative abundances of Bacteroides OTUs were associated with adiposity measures in both dams and offspring. We identified no marked effects of maternal exercise on the gut microbiota of obesogenic diet dams or their offspring. In contrast, maternal exercise decreased gut microbial alpha diversity and altered the abundance of 88 microbial taxa in offspring of control dams. Thirty of these taxa were altered in a similar direction in offspring of sedentary obesogenic vs. control diet dams. In particular, the relative abundances of Oscillibacter OTUs were decreased in offspring of both exercised control dams and sedentary obesogenic diet dams, and associated with blood glucose concentrations and adiposity measures. Analyses of predicted bacterial metabolic pathways inferred decreased indole alkaloid biosynthesis in offspring of both obesogenic diet and exercised control dams. Conclusions: Our data suggest that maternal exercise prior to and during pregnancy resulted in gut dysbiosis in offspring of control dams. Importantly, alterations in the maternal gut microbiota by obesogenic diet or obesity were transferred to their offspring.

Dataset Information

Pregnancy-related changes in the maternal gut microbiota are dependent upon the mother's periconceptional diet.

Publications

Pregnancy-related changes in the maternal gut microbiota are dependent upon the mother's periconceptional diet.

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