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The stepwise assembly of the neonatal virome is modulated by breastfeeding

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Listed:
  • Guanxiang Liang

    (University of Pennsylvania
    Children’s Hospital of Philadelphia)

  • Chunyu Zhao

    (Children’s Hospital of Philadelphia)

  • Huanjia Zhang

    (Children’s Hospital of Philadelphia)

  • Lisa Mattei

    (Children’s Hospital of Philadelphia)

  • Scott Sherrill-Mix

    (University of Pennsylvania)

  • Kyle Bittinger

    (Children’s Hospital of Philadelphia)

  • Lyanna R. Kessler

    (University of Pennsylvania)

  • Gary D. Wu

    (University of Pennsylvania)

  • Robert N. Baldassano

    (Children’s Hospital of Philadelphia)

  • Patricia DeRusso

    (Children’s Hospital of Philadelphia)

  • Eileen Ford

    (Children’s Hospital of Philadelphia)

  • Michal A. Elovitz

    (University of Pennsylvania)

  • Matthew S. Kelly

    (Duke University)

  • Mohamed Z. Patel

    (University of Botswana)

  • Tiny Mazhani

    (University of Botswana)

  • Jeffrey S. Gerber

    (Children’s Hospital of Philadelphia)

  • Andrea Kelly

    (Children’s Hospital of Philadelphia)

  • Babette S. Zemel

    (Children’s Hospital of Philadelphia)

  • Frederic D. Bushman

    (University of Pennsylvania)

Abstract

The gut of healthy human neonates is usually devoid of viruses at birth, but quickly becomes colonized, which—in some cases—leads to gastrointestinal disorders1–4. Here we show that the assembly of the viral community in neonates takes place in distinct steps. Fluorescent staining of virus-like particles purified from infant meconium or early stool samples shows few or no particles, but by one month of life particle numbers increase to 109 per gram, and these numbers seem to persist throughout life5–7. We investigated the origin of these viral populations using shotgun metagenomic sequencing of virus-enriched preparations and whole microbial communities, followed by targeted microbiological analyses. Results indicate that, early after birth, pioneer bacteria colonize the infant gut and by one month prophages induced from these bacteria provide the predominant population of virus-like particles. By four months of life, identifiable viruses that replicate in human cells become more prominent. Multiple human viruses were more abundant in stool samples from babies who were exclusively fed on formula milk compared with those fed partially or fully on breast milk, paralleling reports that breast milk can be protective against viral infections8–10. Bacteriophage populations also differed depending on whether or not the infant was breastfed. We show that the colonization of the infant gut is stepwise, first mainly by temperate bacteriophages induced from pioneer bacteria, and later by viruses that replicate in human cells; this second phase is modulated by breastfeeding.

Suggested Citation

  • Guanxiang Liang & Chunyu Zhao & Huanjia Zhang & Lisa Mattei & Scott Sherrill-Mix & Kyle Bittinger & Lyanna R. Kessler & Gary D. Wu & Robert N. Baldassano & Patricia DeRusso & Eileen Ford & Michal A. E, 2020. "The stepwise assembly of the neonatal virome is modulated by breastfeeding," Nature, Nature, vol. 581(7809), pages 470-474, May.
  • Handle: RePEc:nat:nature:v:581:y:2020:i:7809:d:10.1038_s41586-020-2192-1
    DOI: 10.1038/s41586-020-2192-1
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    Cited by:

    1. Xiaotian Mao & Sabina Birgitte Larsen & Line Sidsel Fisker Zachariassen & Anders Brunse & Signe Adamberg & Josue Leonardo Castro Mejia & Frej Larsen & Kaarel Adamberg & Dennis Sandris Nielsen & Axel K, 2024. "Transfer of modified gut viromes improves symptoms associated with metabolic syndrome in obese male mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Sanzhima Garmaeva & Trishla Sinha & Anastasia Gulyaeva & Nataliia Kuzub & Johanne E. Spreckels & Sergio Andreu-Sánchez & Ranko Gacesa & Arnau Vich Vila & Siobhan Brushett & Marloes Kruk & Jackie Deken, 2024. "Transmission and dynamics of mother-infant gut viruses during pregnancy and early life," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Shuqin Zeng & Alexandre Almeida & Shiping Li & Junjie Ying & Hua Wang & Yi Qu & R. Paul Ross & Catherine Stanton & Zhemin Zhou & Xiaoyu Niu & Dezhi Mu & Shaopu Wang, 2024. "A metagenomic catalog of the early-life human gut virome," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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