Dataset Information

The effects of a set amount of regular maternal exercise during pregnancy on gut microbiota are diet-dependent in mice and do not cause significant diversity changes.

ABSTRACT:

Background

Diet and exercise can affect the gut microbiota (GM); however, the effects of the same amount of exercise on gut microbiota changes in people on a low-fat diet (LFD) and high-fat diet (HFD) during pregnancy are unknown. Do different nutritional conditions respond equally to exercise intervention? This study aimed to investigate the effects of regular maternal exercise during pregnancy on the GM in mice fed different diets during pregnancy.

Methods

Six-week-old nulliparous female KunMing mice were fed either a HFD or LFD before and during pregnancy. Each group of mice were then randomly divided into two groups upon confirmation of pregnancy: sedentary (HFD or LFD; n = 4 and 5, respectively) and exercised (HFDex or LFDex, n = 5 and 6, respectively). Mice were sacrificed on day 19 of gestation and their colon contents were collected. We then performed 16S rDNA gene sequencing of the V3 and V4 regions of the GM.

Results

The pregnancy success rate was 60% for LFDex and 100% for HFDex. Both Chao1 and Simpson indices were not significantly different for either LFD vs. LFDex or HFD vs. HFDex. Desulfobacterota, Desulfovibrionia Desulfovibrionales, Desulfovibrionaceae, Desulfovibrio, Coriobacteriia, Coriobacteriales, and Eggerthellaceae were markedly decreased after exercise intervention in LFDex vs. LFD, whereas Actinobacteria, Bifidobacteriales, Bifidobacteriaceae, Bifidobacterium, and Bifidobacterium pseudolongum were significantly increased in LFDex vs. LFD. Furthermore, decreased Peptostreptococcales-Tissierellales and Peptostreptococcaceae and increased Bacteroides dorei were identified in the HFDex vs. HFD group. p_Desulfobacterota, c_Desulfovibrionia, o_Desulfovibrionales, f_Desulfovibrionaceae and g_Desulfovibrio were markedly decreased in the LFDex group vs. HFDex group.

Conclusions

Our data suggested that quantitative maternal exercise during pregnancy resulted in alterations in GM composition, but did not significantly change the diversity of the GM. These findings may have important implications when considering an individual's overall diet when recommending exercise during pregnancy.

SUBMITTER: Duan X

PROVIDER: S-EPMC9744166 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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Publications

The effects of a set amount of regular maternal exercise during pregnancy on gut microbiota are diet-dependent in mice and do not cause significant diversity changes.

Duan Xia X Xu Jingjing J Yang Ping P Liang Xinyuan X Zeng Zichun Z Luo Huijuan H Tang Xiaomei X Wu Xin X Xiao Xiaomin X

PeerJ 20221202

<h4>Background</h4>Diet and exercise can affect the gut microbiota (GM); however, the effects of the same amount of exercise on gut microbiota changes in people on a low-fat diet (LFD) and high-fat diet (HFD) during pregnancy are unknown. Do different nutritional conditions respond equally to exercise intervention? This study aimed to investigate the effects of regular maternal exercise during pregnancy on the GM in mice fed different diets during pregnancy.<h4>Methods</h4>Six-week-old nulliparo ...[more]

PMID: 36518263

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Project description:IntroductionMaternal obesity poses risks for both mother and offspring during pregnancy, with underlying mechanisms remaining largely unexplored. Obesity is associated with microbial gut dysbiosis and low-grade inflammation, and also the diet has a major impact on these parameters. This study aimed to investigate how maternal obesity and diet contribute to changes in immune responses, exploring potential associations with gut microbiota dysbiosis and adverse pregnancy outcomes in mice.MethodsBefore mating, C57BL/6 mice were assigned to either a high-fat-diet (HFD) or low-fat-diet (LFD) to obtain obese (n=17) and lean (n=10) mice. To distinguish between the effects of obesity and diet, 7 obese mice were switched from the HFD to the LFD from day 7 until day 18 of pregnancy ("switch group"), which was the endpoint of the study. T helper (Th) cell subsets were studied in the spleen, mesenteric lymph nodes (MLN) and Peyer's patches (PP), while monocyte subsets and activation status were determined in maternal blood (flow cytometry). Feces were collected before and during pregnancy (day 7,14,18) for microbiota analysis (16S rRNA sequencing). Pregnancy outcome included determination of fetal and placental weight.ResultsObesity increased splenic Th1 and regulatory T cells, MLN Th1 and PP Th17 cells and enhanced IFN-γ and IL-17A production by splenic Th cells upon ex vivo stimulation. Switching diet decreased splenic and PP Th2 cells and classical monocytes, increased intermediate monocytes and activation of intermediate/nonclassical monocytes. Obesity and diet independently induced changes in the gut microbiota. Various bacterial genera were increased or decreased by obesity or the diet switch. These changes correlated with the immunological changes. Fetal weight was lower in the obese than the lean group, while placental weight was lower in the switch than the obese group.DiscussionThis study demonstrates that obesity and diet independently impact peripheral and intestinal immune responses at the end of pregnancy. Simultaneously, both factors affect specific bacterial gut genera and lead to reduced fetal or placental weight. Our data suggest that switching diet during pregnancy to improve maternal health is not advisable and it supports pre/probiotic treatment of maternal obesity-induced gut dysbiosis to improve maternal immune responses and pregnancy outcome.

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.

Project description:BackgroundMaternal over- and undernutrition in pregnancy plays a critical role in fetal brain development and function. The effects of different maternal diet compositions on intrauterine programing of the fetal brain is a lesser-explored area. The goal of this study was to investigate the impact of two chowmaternal diets on fetal brain gene expression signatures, fetal/neonatal growth, and neonatal and adult behavior in a mouse model.MethodsThroughout pregnancy and lactation, female C57Bl/6J mice were fed one of two standard, commercially available chow diets (pellet versus powder). The powdered chow diet was relatively deficient in micronutrients and enriched for carbohydrates and n-3 long-chain polyunsaturated fatty acids compared to the pelleted chow. RNA was extracted from embryonic day 15.5 forebrains and hybridized to whole genome expression microarrays (N = 5/maternal diet group). Functional analyses of significantly differentially expressed fetal brain genes were performed using Ingenuity Pathways Analysis and Gene Set Enrichment Analysis. Neonatal behavior was assessed using a validated scale (N = 62 pellet-exposed and 31 powder-exposed). Hippocampal learning, locomotor behavior, and motor coordination were assessed in a subset of adults using fear conditioning, open field testing, and Rotarod tests (N = 16 pellet-exposed, 14 powder-exposed).ResultsComparing powdered to pelleted chow diets, neither maternal weight trajectory in pregnancy nor embryo size differed. Maternal powdered chow diet was associated with 1647 differentially expressed fetal brain genes. Functional analyses identified significant upregulation of canonical pathways and upstream regulators involved in cell cycle regulation, synaptic plasticity, and sensory nervous system development in the fetal brain, and significant downregulation of pathways related to cell and embryo death. Pathways related to DNA damage response, brain immune response, amino acid and fatty acid transport, and dopaminergic signaling were significantly dysregulated. Powdered chow-exposed neonates were significantly longer but not heavier than pelleted chow-exposed counterparts. On neonatal behavioral testing, powdered chow-exposed neonates achieved coordination- and strength-related milestones significantly earlier, but sensory maturation reflexes significantly later. On adult behavioral testing, powdered chow-exposed offspring exhibited hyperactivity and hippocampal learning deficits.ConclusionIn wild-type offspring, two diets that differed primarily with respect to micronutrient composition had significant effects on the fetal brain transcriptome, neonatal and adult behavior. These effects did not appear to be mediated by alterations in gross maternal nutritional status nor fetal/neonatal weight. Maternal dietary content is an important variable to consider for investigators evaluating fetal brain development and offspring behavior.

Project description:Early-life overnutrition programs increased risks of metabolic disorders in adulthood. Regular exercise has been widely accepted to be an effective measure to maintain metabolic health. However, the intergenerational effects of maternal exercise and the specific mechanism are largely unclear. Our objective was to investigate whether maternal exercise could alleviate the metabolic disturbances induced by early-life overnutrition in both dams and offspring and to explore the role of gut microbiota in mediating the effects. C57BL/6 female mice were randomly divided into three groups: the control group, which were fed a normal control diet; high-fat group, which received a high-fat diet; and high-fat with exercise intervention group, which was fed a high-fat diet and received a voluntary wheel running training. The diet intervention started from 3 weeks prior to mating and lasted throughout pregnancy and lactation. The exercise intervention was only prior to and during pregnancy. The male offspring got free access to normal chow diet from weaning to 24 weeks of age. Glucose tolerance test and biochemical parameters were detected in dams at weaning and offspring at 8 and 24 weeks of age. Their cecal contents were collected for the 16 s rDNA amplicon sequencing. The results showed that maternal high-fat diet resulted in significant glucose intolerance, insulin resistance, and lipid profiles disorders in both dams and offspring. Maternal exercise markedly improved insulin sensitivity in dams and metabolic disorders in offspring from young into adulthood. The decrease in unfavorable bacteria and the persistent enrichment of short-chain fatty acids-producers from mothers to adult offspring, particularly the genus Odoribacter, were all associated with the improvement of metabolism by maternal exercise. Overall, maternal exercise could significantly mitigate the detrimental effects of a maternal high-fat diet on metabolism in both dams and male offspring. The continuous alterations in gut microbiota might be a critical factor in deciphering the metabolic benefits of maternal exercise, which provides some novel evidence and targets for combating metabolic diseases.

Dataset Information

The effects of a set amount of regular maternal exercise during pregnancy on gut microbiota are diet-dependent in mice and do not cause significant diversity changes.

Background

Methods

Results

Conclusions

Publications

The effects of a set amount of regular maternal exercise during pregnancy on gut microbiota are diet-dependent in mice and do not cause significant diversity changes.

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