The stepwise assembly of the neonatal virome is modulated by breastfeeding

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. Elovitz, Matthew S. Kelly, Mohamed Z. Patel, Tiny Mazhani, Jeffrey S. Gerber, Andrea Kelly, Babette S. Zemel and Frederic D. Bushman ()
Additional contact information
Guanxiang Liang: University of Pennsylvania
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

Nature, 2020, vol. 581, issue 7809, 470-474

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41586-020-2192-1

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