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Transmission and dynamics of mother-infant gut viruses during pregnancy and early life

Author

Listed:
  • Sanzhima Garmaeva

    (University of Groningen, University Medical Center Groningen)

  • Trishla Sinha

    (University of Groningen, University Medical Center Groningen)

  • Anastasia Gulyaeva

    (University of Groningen, University Medical Center Groningen)

  • Nataliia Kuzub

    (University of Groningen, University Medical Center Groningen)

  • Johanne E. Spreckels

    (University of Groningen, University Medical Center Groningen)

  • Sergio Andreu-Sánchez

    (University of Groningen, University Medical Center Groningen
    University of Groningen, University Medical Center Groningen)

  • Ranko Gacesa

    (University of Groningen, University Medical Center Groningen
    University of Groningen, University Medical Center Groningen)

  • Arnau Vich Vila

    (University of Groningen, University Medical Center Groningen
    University of Groningen, University Medical Center Groningen)

  • Siobhan Brushett

    (University of Groningen, University Medical Center Groningen
    University of Groningen, University Medical Center Groningen)

  • Marloes Kruk

    (University of Groningen, University Medical Center Groningen)

  • Jackie Dekens

    (University of Groningen, University Medical Center Groningen
    University Medical Center Groningen, Center for Development and Innovation)

  • Jan Sikkema

    (University Medical Center Groningen, Center for Development and Innovation)

  • Folkert Kuipers

    (University of Groningen, University Medical Center Groningen
    European Research Institute for the Biology of Ageing (ERIBA), University of Groningen, University Medical Center Groningen)

  • Andrey N. Shkoporov

    (APC Microbiome Ireland, University College Cork
    University College Cork)

  • Colin Hill

    (APC Microbiome Ireland, University College Cork
    University College Cork)

  • Sicco Scherjon

    (University of Groningen, University Medical Center Groningen)

  • Cisca Wijmenga

    (University of Groningen, University Medical Center Groningen)

  • Jingyuan Fu

    (University of Groningen, University Medical Center Groningen
    University of Groningen, University Medical Center Groningen)

  • Alexander Kurilshikov

    (University of Groningen, University Medical Center Groningen)

  • Alexandra Zhernakova

    (University of Groningen, University Medical Center Groningen)

Abstract

Early development of the gut ecosystem is crucial for lifelong health. While infant gut bacterial communities have been studied extensively, the infant gut virome remains under-explored. To study the development of the infant gut virome over time and the factors that shape it, we longitudinally assess the composition of gut viruses and their bacterial hosts in 30 women during and after pregnancy and in their 32 infants during their first year of life. Using shotgun metagenomic sequencing applied to dsDNA extracted from Virus-Like Particles (VLPs) and bacteria, we generate 205 VLP metaviromes and 322 total metagenomes. With this data, we show that while the maternal gut virome composition remains stable during late pregnancy and after birth, the infant gut virome is dynamic in the first year of life. Notably, infant gut viromes contain a higher abundance of active temperate phages compared to maternal gut viromes, which decreases over the first year of life. Moreover, we show that the feeding mode and place of delivery influence the gut virome composition of infants. Lastly, we provide evidence of co-transmission of viral and bacterial strains from mothers to infants, demonstrating that infants acquire some of their virome from their mother’s gut.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45257-4
    DOI: 10.1038/s41467-024-45257-4
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    1. Mireia Valles-Colomer & Aitor Blanco-Míguez & Paolo Manghi & Francesco Asnicar & Leonard Dubois & Davide Golzato & Federica Armanini & Fabio Cumbo & Kun D. Huang & Serena Manara & Giulia Masetti & Fed, 2023. "The person-to-person transmission landscape of the gut and oral microbiomes," Nature, Nature, vol. 614(7946), pages 125-135, February.
    2. Katherine M. Kennedy & Marcus C. Goffau & Maria Elisa Perez-Muñoz & Marie-Claire Arrieta & Fredrik Bäckhed & Peer Bork & Thorsten Braun & Frederic D. Bushman & Joel Dore & Willem M. Vos & Ashlee M. Ea, 2023. "Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies," Nature, Nature, vol. 613(7945), pages 639-649, January.
    3. 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.
    4. Natalya Yutin & Sean Benler & Sergei A. Shmakov & Yuri I. Wolf & Igor Tolstoy & Mike Rayko & Dmitry Antipov & Pavel A. Pevzner & Eugene V. Koonin, 2021. "Analysis of metagenome-assembled viral genomes from the human gut reveals diverse putative CrAss-like phages with unique genomic features," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    5. Tanya Yatsunenko & Federico E. Rey & Mark J. Manary & Indi Trehan & Maria Gloria Dominguez-Bello & Monica Contreras & Magda Magris & Glida Hidalgo & Robert N. Baldassano & Andrey P. Anokhin & Andrew C, 2012. "Human gut microbiome viewed across age and geography," Nature, Nature, vol. 486(7402), pages 222-227, June.
    6. Christopher J. Stewart & Nadim J. Ajami & Jacqueline L. O’Brien & Diane S. Hutchinson & Daniel P. Smith & Matthew C. Wong & Matthew C. Ross & Richard E. Lloyd & HarshaVardhan Doddapaneni & Ginger A. M, 2018. "Temporal development of the gut microbiome in early childhood from the TEDDY study," Nature, Nature, vol. 562(7728), pages 583-588, October.
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