Abstract
The microbiome is a regulator of host immunity, metabolism, neurodevelopment, and behavior. During early life, bacterial communities within maternal gut and vaginal compartments can have an impact on directing these processes. Maternal stress experience during pregnancy may impact offspring development by altering the temporal and spatial dynamics of the maternal microbiome during pregnancy. To examine the hypothesis that maternal stress disrupts gut and vaginal microbial dynamics during critical prenatal and postnatal windows, we used high-resolution 16S rRNA marker gene sequencing to examine outcomes in our mouse model of early prenatal stress. Consistent with predictions, maternal fecal communities shift across pregnancy, a process that is disrupted by stress. Vaginal bacterial community structure and composition exhibit lasting disruption following stress exposure. Comparison of maternal and offspring microbiota revealed that similarities in bacterial community composition was predicted by a complex interaction between maternal body niche and offspring age and sex. Importantly, early prenatal stress influenced offspring bacterial community assembly in a temporal and sex-specific manner. Taken together, our results demonstrate that early prenatal stress may influence offspring development through converging modifications to gut microbial composition during pregnancy and transmission of dysbiotic vaginal microbiome at birth.
Highlights
Maternal nutritional status influences placental function, alterations to the structure and metabolic potential of the maternal bacterial microbiome may represent a currently uncharacterized association through which maternal stress experience impacts offspring outcomes[28,29]
Life host-microbe interactions disproportionally contribute to later health outcomes including susceptibility and resistance to infection, predisposition to inflammatory and metabolic disorders, and changes to neural circuits that control stress and affect, yet remarkably little is known about the maternal factors that may influence this process[19,54,55,56,57,58,59,60]
Maternal stress experience during pregnancy is associated with profound dysregulation of pathways along the gut-brain axis, far less is known regarding the direct impact of stress on maternal bacterial communities that, in turn, shape these health outcomes in offspring[15,16,17,18,30,61,62,63,64,65]
Summary
Maternal nutritional status influences placental function, alterations to the structure and metabolic potential of the maternal bacterial microbiome may represent a currently uncharacterized association through which maternal stress experience impacts offspring outcomes[28,29]. To examine the hypothesis that maternal stress experience disrupts gut and vaginal microbial dynamics during critical prenatal and postnatal windows, we used a high-resolution sampling strategy coupled with 16S rRNA marker gene sequencing to examine outcomes in our mouse model of early prenatal stress, in which male, but not female, offspring demonstrate significant neurodevelopmental changes in hypothalamic and limbic circuits and in the regulation of stress responsivity, cognitive dysfunction, and post-pubertal growth[18,25,26,45,46,47,48] This approach provides an opportunity to draw novel associations between the effects of stress during pregnancy on the structure and functional potential of maternal bacterial communities and sex-specific phenotypes that emerge in offspring as adults. These studies provide an in-depth timeline reconstruction of temporal and spatial kinetics of maternal microbial communities following stress exposure and subsequent influence on the assembly of offspring microbial communities
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