The composition of human vaginal microbiota transferred at birth affects offspring health in a mouse model

doi:10.1038/s41467-021-26634-9

. 2021 Nov 1;12(1):6289.

doi: 10.1038/s41467-021-26634-9.

The composition of human vaginal microbiota transferred at birth affects offspring health in a mouse model

Eldin Jašarević^{1

2

3}, Elizabeth M Hill^{1

2}, Patrick J Kane^{1

2}, Lindsay Rutt^{4

5}, Trevonn Gyles^{1

2}, Lillian Folts^{1

2}, Kylie D Rock^{1

2}, Christopher D Howard^{1

2}, Kathleen E Morrison^{1

2}, Jacques Ravel^{4

5}, Tracy L Bale^{6

7

8}

Affiliations

¹ Center for Epigenetic Research in Child Health and Brain Development, University of Maryland, School of Medicine, Baltimore, MD, 21201, USA.
² Department of Pharmacology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
³ Department of Obstetrics, Gynecology and Reproductive Sciences, Magee-Womens Research Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15213, USA.
⁴ Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
⁵ Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
⁶ Center for Epigenetic Research in Child Health and Brain Development, University of Maryland, School of Medicine, Baltimore, MD, 21201, USA. [email protected].
⁷ Department of Pharmacology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA. [email protected].
⁸ Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, 21201, USA. [email protected].

PMID: 34725359
PMCID: PMC8560944
DOI: 10.1038/s41467-021-26634-9

The composition of human vaginal microbiota transferred at birth affects offspring health in a mouse model

Eldin Jašarević et al. Nat Commun. 2021.

. 2021 Nov 1;12(1):6289.

doi: 10.1038/s41467-021-26634-9.

Authors

Affiliations

¹ Center for Epigenetic Research in Child Health and Brain Development, University of Maryland, School of Medicine, Baltimore, MD, 21201, USA.
² Department of Pharmacology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
³ Department of Obstetrics, Gynecology and Reproductive Sciences, Magee-Womens Research Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15213, USA.
⁴ Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
⁵ Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
⁶ Center for Epigenetic Research in Child Health and Brain Development, University of Maryland, School of Medicine, Baltimore, MD, 21201, USA. [email protected].
⁷ Department of Pharmacology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA. [email protected].
⁸ Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, 21201, USA. [email protected].

PMID: 34725359
PMCID: PMC8560944
DOI: 10.1038/s41467-021-26634-9

Abstract

Newborns are colonized by maternal microbiota that is essential for offspring health and development. The composition of these pioneer communities exhibits individual differences, but the importance of this early-life heterogeneity to health outcomes is not understood. Here we validate a human microbiota-associated model in which fetal mice are cesarean delivered and gavaged with defined human vaginal microbial communities. This model replicates the inoculation that occurs during vaginal birth and reveals lasting effects on offspring metabolism, immunity, and the brain in a community-specific manner. This microbial effect is amplified by prior gestation in a maternal obesogenic or vaginal dysbiotic environment where placental and fetal ileum development are altered, and an augmented immune response increases rates of offspring mortality. Collectively, we describe a translationally relevant model to examine the defined role of specific human microbial communities on offspring health outcomes, and demonstrate that the prenatal environment dramatically shapes the postnatal response to inoculation.

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Conflict of interest statement

J.R. is Founder and Chief Scientist at LUCA Biologics. The remaining authors declare no competing interests.

Figures

**Fig. 1. Exposure at birth to distinct maternal microbiota on offspring growth, circulating immunity, and hypothalamic gene expression patterns.**
A Schematic of the experimental timeline and protocol used to establish a mouse model to investigate the impact of exposure to maternal human vaginal microbiota at birth on lasting offspring outcomes. See Methods and accompanying Supplementary Fig. 1 for additional details. Created with BioRender.com. B Validation of presence of human vaginal microbiota across intestinal segments of C-section neonate mice inoculated with *L. crispatus-*dominated microbiota (CST I) or lactobacilli-deficient, nonoptimal microbiota (CST IV) collected from late-gestation women using 16 S rRNA gene marker sequencing. Upper left panel, mean relative abundance of *L. crispatus* showing no detectable amplification of *L. crispatus* in the Amies transport medium and CST IV samples. Upper middle and right panel, mean relative abundance of *L. crispatus* in CST I inoculated offspring at postnatal day 1 and 2. No amplification of *L. crispatus* was detected in Amies and CST IV inoculated pups at either timepoint. Lower left panel, mean relative abundance from CST IV associated taxa showing no detectable amplification in the Amies transport medium and CST I samples. Upper middle and right panel, mean relative abundance of CST IV inoculated offspring at postnatal day 1 and 2. No amplification of CST IV was detected in Amies, and CST I inoculated pups at either timepoint. N = 7–20 per group and intestinal segment. C Sex-specific effects of CST I and CST IV inoculation on body weight across development. Top panel, male body weight was significantly changed over time (two-way ANOVA, main effect of time F_{5, 170} = 689.4, P < 0.0001) and the interaction between time and treatment (two-way ANOVA, time*treatment interaction, F_{15, 170} = 8.544, P < 0.0001). Tukey’s post-hoc analysis revealed that CST IV males weighed more than Amies and CST I males at P56 (Tukey’s, P = 0.0009 and 0.0006, respectively). No differences in body weight in CST I males compared with Amies or vaginally delivered males at P56 (Tukey’s, P = 0.990 and P = 0.261). Bottom panel, female body weight was significantly changed over time (two-way ANOVA, main effect of time F_{5, 130} = 306.819, P < 0.0001). No effect of treatment or their interaction was observed. Males: N = 7 Amies, 12 CST I, 11 CST IV, 7 vaginally delivered per timepoint. Females: N = 8 Amies, 9 CST I, 7 CST IV, 6 vaginally delivered per timepoint. Data represented as mean ± SEM. Data are representative of two independent experiments. ***P < 0.001. D–F High-dimensional, single-cell mapping reveals lasting effects of CST I and CST IV inoculation on the circulating immune compartment in adult males. D t-Distributed stochastic neighbor embedding (t-SNE) visualization demonstrating CyTOF assessment of CD45+ immune cells in whole blood of CST I, CST IV, and vaginally delivered postnatal day 56 adult males (equal sampling across treatment groups, total 390,000 events). E Average frequencies of major leukocytes within whole blood in CST I, CST IV, and VD adult males. F Frequencies of circulating innate immune cells showing increased frequency of neutrophils in CST I and CST IV males compared with VD males at P56 (two-way ANOVA, treatment*immune cell interaction, F_{8, 56} = 2.870, P = 0.0095; Tukey’s post-hoc CST I vs VD P = 0.0001; Tukey’s post-hoc CST IV vs VD P = 0.0003). N = 7 CST I males, 3 CST IV males, 7 vaginally delivered males. Data represented as mean ± SEM with individual data points overlaid. ***P < 0.001. G Frequencies of circulating adaptive immune cells showing decreased frequency of B220 + B cells in CST I males compared with VD males at P56 (two-way ANOVA, treatment*immune cell interaction, F_{6, 56} = 2.492, P = 0.0330; Tukey’s post-hoc CST I vs. VD P = 0.0003). N = 7 CST I males, 3 CST IV males, 7 vaginally delivered males. Data represented as mean ± SEM with individual data points overlaid. ***P < 0.001. H Frequencies of circulating B220⁺ B cells showing decreased frequency of B220⁺IgD⁺ B cells in CST I males compared with VD males (two-way ANOVA, treatment*immune cell interaction, F_{4, 28} = 5.471, P = 0.0022; Tukey’s post-hoc CST I vs. VD P = 0.0017). N = 7 CST I males, 3 CST IV males, 7 vaginally delivered males Data represented as mean ± SEM with individual data points overlaid. ***P < 0.001. I Heatmap depicting mean expression of genes in the paraventricular nucleus of the hypothalamus in P56 males. Paralleling body weight differences between CST I and CST IV males at P56, RNA-seq analysis shows differences in PVN gene expression patterns between CST I and CST IV males (linear fit model, FDR < 0.1, log(FC) = 1.5). Unbiased hierarchical clustering showing similarity in transcriptional patterns between CST IV and VD males, and CST I and Amies males. Color based on row Z-scores for each gene. Three clusters of differentially regulated genes in each treatment group are indicated. N = 4–6 males per treatment. J Cluster-based functional enrichment analysis of differentially expressed genes in the paraventricular nucleus of the hypothalamus in P56 males. Significant enrichment of pathways involved in metabolism and immunity in CST IV compared with CST I males, showing unique pathways in the PVN that are associated with body weight changes in CST IV males (FDR < 0.05). Bubble plot size denotes enrichment. Clusters identified in differential gene expression analysis were used for this pathway enrichment and color-coded as blue (Cluster 1), orange (Cluster 2) and pink (Cluster 3). N = 4–6 males per treatment.

**Fig. 2. Transcriptional landscape of the neonatal ileum and the circulating immune compartment is influenced by vaginal community state type.**
A Schematic of experimental outline to determine the influence of the human microbiome on transcriptional profiles of the neonatal ileum and the circulating immune compartment. Created with BioRender.com. B Principal component analysis plots of gene expression data demonstrating the distribution of P1 male ileum samples colored by treatment group, revealing clustering is driven by developmental maturity, mode of delivery, and colonization (C-section Amies inoculated vs. vaginally delivered) and the C-section pups inoculated with human vaginal microbiota as an intermediate between the Amies and vaginally delivered pups. P1 corresponds to 24 hrs post-inoculation. N = 3–4 males per treatment. C Heatmap depicting mean expression of genes in the ileum P1 males, showing differences between CST I and CST IV males (linear fit model, FDR < 0.1, log(FC) = 1.5). Unbiased hierarchical clustering showing similarity in transcriptional patterns between CST IV and VD males, and CST I and Amies males. P1 corresponds to 24 h post-inoculation. Color based on row Z-scores for each gene. Three clusters of differentially regulated genes in each treatment group are indicated. N = 3–4 males per treatment. D Cluster-based functional enrichment analysis of differentially expressed genes in the ileum of P1 males showing significant enrichment of pathways involved in defense response to bacteria, innate immune activation, chemotaxis, and mucus secretion in the ileum of CST IV relative to CST I inoculated males (FDR < 0.05). Bubble plot size denotes enrichment. N = 4–6 males per treatment. E t-SNE visualization demonstrating CyTOF phenotyping of CD45+ immune cells in whole blood of CST I, CST IV, and vaginally delivered males showing neutrophils as the major immune subset in the circulating immune compartment at P1 (equal sampling across treatment groups, total 10,000 events). P1 corresponds to 24 h post-inoculation. N = 3 males per treatment. F Average frequencies of major leukocytes within whole blood in P1 CST I, CST IV, and VD males. N = 3 males per treatment. G–L Frequencies of circulating (G) neutrophils, (H) monocytes, (I) MHC II⁺ B cells, (J) MHC II^- B cells, K CD8 + T cells, and L CD4⁺ T cells within whole blood in P1 CST I, CST IV, and VD males. (1) Frequency of CD4⁺ T cells were significantly increased in VD males compared with CST I and CST IV males (One-way ANOVA, F_2,6 = 15.97, P = 0.0040; Tukey’s post-hoc CST I vs. VD P = 0.0072; CST IV vs. VD P = 0.0059). N = 3 males per treatment. Data represented as mean ± SEM with individual data points overlaid. **P < 0.01.

**Fig. 3. Modeling compounding maternal risk factors results in an adverse response to birth-associated microbial exposure.**
A Schematic of experimental timeline for the induction of pregestational excessive weight gain, glucose intolerance, and microbiota alterations through the consumption of a high-fat low-fiber diet (HFt-LFb). Day 0 refers to the beginning of the dietary treatment and does not reflect chronological age. Created with BioRender.com. B Consumption of a high-fat low-fiber diet accelerates body weight gain in females compared with females consuming a low-fat high-fiber diet (two-way ANOVA, main effect of time, F_{5, 120} = 94.17, P < 0.0001; main effect of diet, F_{1, 24} = 30.70, P < 0.0001; time*diet interaction, F_{5, 120} = 36.61, P < 0.0001). N = 12 LFt-HFb females, 20 HFt-LFb females per timepoint. Data represented as mean ± SEM. Time (in weeks) is measured from time of diet switch. Data are representative of two independent experiments. **P < 0.01, ***P < 0.001. C Principal coordinates analysis demonstrating temporal dynamics of diet on the gut microbiota, whereby 1wk consumption of a high-fat low-fiber diet resulted in separate clustering from females consuming a low-fat high-fiber diet that failed to recover during the treatment window. N = 12 LFt-HFb females, 20 HFt-LFb females per timepoint, total of 68 samples that passed quality filtering. D Mean relative abundance of top ten taxa showing rapid changes to the fecal microbiota following transition to a high-fat low-fat diet, characterized by a loss of Clostridiales. N = 12 LFt-HFb females, 20 HFt-LFb females per timepoint, total of 68 samples that passed quality filtering. E Expression of HIF-1a is significantly decreased in the colon following 6-week consumption of a high-fat low-fiber diet relative to females consuming a low-fat high-fiber diet (two-sided t-test, t₄ = 4.9, P = 0.008), indicating possible disruption in hypoxia homeostasis in the colon. N = 3 LFt-HFb females, 3 HFt-LFb females. Data represented as mean ± SEM with individual data points overlaid. **P < 0.01. F Left, Plasma glucose levels during a glucose tolerance test in females consuming either a high-fat low-fiber or low-fat high-fiber diet. Females consuming a high-fat low-fiber diet showed significant delay in glucose clearance (two-way ANOVA, main effect of time, F_{4, 108} = 106.33, P < 0.0001; main effect of diet, F_{1, 27} = 15.86, P = 0.0005; time*diet interaction, F_{4, 108} = 15.44, P < 0.0001). Right, AUC of total plasma glucose levels showing increase glucose levels in females consuming a high-fat low-fiber diet (two-tailed t-test, t₂₄ = 4.055, P = 0.005). N = 9 LFt-HFb females, 17 HFt-LFb females Data represented as mean ± SD with individual data points overlaid. ***P < 0.001. G Schematic of experimental design to determine the impact of prenatal exposure to compounding maternal adversities, such as diet and presence of a common member of CST IV, during pregnancy on offspring outcomes. We induced the pregestational phenotype and colonized pregnant females to *G. vaginalis* 11E4 (Gv) gestational day 13.5 and 15.5. At gestational day 18.5, offspring from all treatment groups were colonized with the nonoptimal CST IV human vaginal microbiota. Created with BioRender.com. H Survival of offspring from dams that experience a single or multiple compounding adversities. All pups were C-section delivered and gavaged with human CST IV inoculant, showing the highest offspring mortality risk in HFt-LFb+Gv offspring that were exposed to CST IV at birth. LFt-HFb = low-fat high-fiber; HFt-LFb = high-fat low-fiber; Gv = *G. vaginalis* 11E4. Kaplan–Meier survival analysis. N = 20 offspring per treatment condition. I Compounding effects of maternal diet, maternal vaginal colonization by *G. vaginalis* (Gv), and exposure to CST IV on absolute number of neutrophils in the circulation of postnatal day 1 male pups. Triple-hit male pups show significant increase in neutrophils compared with vaginally delivered and CST IV inoculated offspring (One-way ANOVA, main effect of treatment, F_{3, 11} = 8.452, P = 0.0034; VD vs. Triple Hit, P = 0.0188; CST IV vs. Triple Hit, P = 0.0026). N = 3 vaginally delivered males, 5 CST IV inoculated LFt-HFb males, 4 CST IV inoculated HFt-LFb males, 3 CST IV inoculated HFt-LFb+Gv males. Data represented as mean ± SEM with individual data points overlaid. *P < 0.05, **P < 0.01.

**Fig. 4. Prenatal exposure to maternal diet-induced obesity and a nonoptimal vaginal microbiota alter the transcriptional landscape in the placenta and fetal ileum of male offspring.**
A Schematic of experimental design to determine whether compounding maternal adversities, such as diet and *G. vaginalis* vaginal colonization, impact fetal development that may contribute to increased offspring mortality risk. We induced the pregestational phenotype and dams were colonized with *G. vaginalis* 11E4 on gestational day 13.5 and 15.5. At gestational day 18.5, tissue from one cohort of male offspring was collected for analysis of gene expression patterns in the placenta and ileum. A second cohort of offspring were colonized with the nonoptimal CST IV human vaginal microbiota. Created with BioRender.com. B Venn diagram displaying the number of differentially expressed genes in the embryonic day 18.5 placenta of male offspring exposed to a maternal high-fat low-fiber diet, *G. vaginalis* 11E4 vaginal colonization, or a combination (linear fit model, FDR < 0.1, log(FC) = 1.5; n = 351 genes). LFt-HFb = low-fat high-fiber; HFt-LFb = high-fat low-fiber; Gv = *G. vaginalis* 11E4. C Heatmap depicting mean expression of genes in the placenta of embryonic day 18.5 male offspring exposed to a maternal high-fat low-fiber diet, *G. vaginalis* 11E4 vaginal colonization, or a combination (HFt-LFb+Gv) (linear fit model, FDR < 0.1, log(FC) = 1.5). These comparisons reveal a unique cluster of genes that are differentially expressed in HFt-LFb+Gv male placenta compared with other treatment groups. Z-scores plotted across individuals for each gene. LFt-HFb = low-fat high-fiber; HFt-LFb = high-fat low-fiber; Gv = *G. vaginalis* 11E4. Color based on row Z-scores for each gene. Six clusters of differentially regulated genes in each treatment group are indicated. N = 3 males per treatment. D Venn diagram displaying the number of differentially expressed genes in the embryonic day 18.5 ileum of male offspring exposed to a maternal high-fat low-fiber diet, *G. vaginalis* 11E4 vaginal colonization, or a combination (HFt-LFb+Gv) These comparisons reveal a unique cluster of genes that are differentially expressed in the fetal ileum of HFt-LFb+Gv males compared with other treatment groups (linear fit model, FDR < 0.1, log(FC) = 1.5; n = 781 genes). LFt-HFb = low-fat high-fiber; HFt-LFb = high-fat low-fiber; Gv = *G. vaginalis* 11E4. E Heatmap depicting mean expression of genes in the ileum of embryonic day 18.5 male offspring exposed to a maternal high-fat low-fiber diet, *G. vaginalis* 11E4 vaginal colonization, or a combination (linear fit model, FDR < 0.1, log(FC) = 1.5). Color based on row Z-scores for each gene. Five clusters of differentially regulated genes in each treatment group are indicated. N = 3 males per treatment. F Survival of offspring from dams that experience a single or multiple compounding adversities in a second validation cohort. All pups were C-section delivered and gavaged with human CST IV inoculant, showing the highest offspring mortality risk in HFt-LFb+Gv male offspring exposed to CST IV at birth. LFt-HFb = low-fat high-fiber; HFt-LFb = high-fat low-fiber; Gv = *G. vaginalis* 11E4. Kaplan–Meier survival analysis. N = 24–40 offspring per treatment condition.

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References

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[1] Funkhouser LJ, Bordenstein SR. Mom knows best: The Universality of Maternal Microbial Transmission. PLoS Biol. 2013;11:e1001631. doi: 10.1371/journal.pbio.1001631. - DOI - PMC - PubMed

[2] Funkhouser LJ, Bordenstein SR. Mom knows best: The Universality of Maternal Microbial Transmission. PLoS Biol. 2013;11:e1001631. doi: 10.1371/journal.pbio.1001631. - DOI - PMC - PubMed

[3] Metcalf, C. J. E., Henry, L. P., Rebolleda-Gómez, M. & Koskella, B. Why evolve reliance on the microbiome for timing of ontogeny? mBio10, e01496–19 (2019). - PMC - PubMed

[4] Metcalf, C. J. E., Henry, L. P., Rebolleda-Gómez, M. & Koskella, B. Why evolve reliance on the microbiome for timing of ontogeny? mBio10, e01496–19 (2019). - PMC - PubMed

[5] Ferretti P, et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe. 2018;24:133–145.e5. doi: 10.1016/j.chom.2018.06.005. - DOI - PMC - PubMed

[6] Ferretti P, et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe. 2018;24:133–145.e5. doi: 10.1016/j.chom.2018.06.005. - DOI - PMC - PubMed

[7] Arrieta M-C, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 2015;7:307ra152–307ra152. doi: 10.1126/scitranslmed.aab2271. - DOI - PubMed

[8] Arrieta M-C, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 2015;7:307ra152–307ra152. doi: 10.1126/scitranslmed.aab2271. - DOI - PubMed

[9] Fulde M, et al. Neonatal selection by Toll-like receptor 5 influences long-term gut microbiota composition. Nature. 2018;560:489–493. doi: 10.1038/s41586-018-0395-5. - DOI - PubMed

[10] Fulde M, et al. Neonatal selection by Toll-like receptor 5 influences long-term gut microbiota composition. Nature. 2018;560:489–493. doi: 10.1038/s41586-018-0395-5. - DOI - PubMed

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The composition of human vaginal microbiota transferred at birth affects offspring health in a mouse model

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The composition of human vaginal microbiota transferred at birth affects offspring health in a mouse model

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