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

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Listed:
  • Eldin Jašarević

    (University of Maryland, School of Medicine
    University of Maryland School of Medicine
    University of Pittsburgh School of Medicine)

  • Elizabeth M. Hill

    (University of Maryland, School of Medicine
    University of Maryland School of Medicine)

  • Patrick J. Kane

    (University of Maryland, School of Medicine
    University of Maryland School of Medicine)

  • Lindsay Rutt

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

  • Trevonn Gyles

    (University of Maryland, School of Medicine
    University of Maryland School of Medicine)

  • Lillian Folts

    (University of Maryland, School of Medicine
    University of Maryland School of Medicine)

  • Kylie D. Rock

    (University of Maryland, School of Medicine
    University of Maryland School of Medicine)

  • Christopher D. Howard

    (University of Maryland, School of Medicine
    University of Maryland School of Medicine)

  • Kathleen E. Morrison

    (University of Maryland, School of Medicine
    University of Maryland School of Medicine)

  • Jacques Ravel

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

  • Tracy L. Bale

    (University of Maryland, School of Medicine
    University of Maryland School of Medicine
    University of Maryland School of Medicine)

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.

Suggested Citation

  • Eldin Jašarević & Elizabeth M. Hill & Patrick J. Kane & Lindsay Rutt & Trevonn Gyles & Lillian Folts & Kylie D. Rock & Christopher D. Howard & Kathleen E. Morrison & Jacques Ravel & Tracy L. Bale, 2021. "The composition of human vaginal microbiota transferred at birth affects offspring health in a mouse model," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26634-9
    DOI: 10.1038/s41467-021-26634-9
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    References listed on IDEAS

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    1. Naomi McGovern & Amanda Shin & Gillian Low & Donovan Low & Kaibo Duan & Leong Jing Yao & Rasha Msallam & Ivy Low & Nurhidaya Binte Shadan & Hermi R Sumatoh & Erin Soon & Josephine Lum & Esther Mok & S, 2017. "Human fetal dendritic cells promote prenatal T-cell immune suppression through arginase-2," Nature, Nature, vol. 546(7660), pages 662-666, June.
    2. Helen E. Vuong & Geoffrey N. Pronovost & Drake W. Williams & Elena J. L. Coley & Emily L. Siegler & Austin Qiu & Maria Kazantsev & Chantel J. Wilson & Tomiko Rendon & Elaine Y. Hsiao, 2020. "The maternal microbiome modulates fetal neurodevelopment in mice," Nature, Nature, vol. 586(7828), pages 281-286, October.
    3. Atara Uzan-Yulzari & Olli Turta & Anna Belogolovski & Oren Ziv & Christina Kunz & Sarah Perschbacher & Hadar Neuman & Edoardo Pasolli & Aia Oz & Hila Ben-Amram & Himanshu Kumar & Helena Ollila & Anne , 2021. "Neonatal antibiotic exposure impairs child growth during the first six years of life by perturbing intestinal microbial colonization," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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