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A metagenomic catalog of the early-life human gut virome

Author

Listed:
  • Shuqin Zeng

    (West China Second University Hospital, Sichuan University
    West China Second University Hospital, Sichuan University)

  • Alexandre Almeida

    (University of Cambridge)

  • Shiping Li

    (West China Second University Hospital, Sichuan University
    West China Second University Hospital, Sichuan University)

  • Junjie Ying

    (West China Second University Hospital, Sichuan University
    West China Second University Hospital, Sichuan University)

  • Hua Wang

    (West China Second University Hospital, Sichuan University
    West China Second University Hospital, Sichuan University)

  • Yi Qu

    (West China Second University Hospital, Sichuan University
    West China Second University Hospital, Sichuan University)

  • R. Paul Ross

    (APC Microbiome Ireland, University College Cork)

  • Catherine Stanton

    (APC Microbiome Ireland, University College Cork
    Teagasc Food Research Centre, Moorepark, Fermoy)

  • Zhemin Zhou

    (Pasteurien College, Medical College of Soochow University, Soochow University)

  • Xiaoyu Niu

    (West China Second University Hospital, Sichuan University
    West China Second University Hospital, Sichuan University)

  • Dezhi Mu

    (West China Second University Hospital, Sichuan University
    West China Second University Hospital, Sichuan University)

  • Shaopu Wang

    (West China Second University Hospital, Sichuan University
    West China Second University Hospital, Sichuan University)

Abstract

Early-life human gut microbiome is a pivotal driver of gut homeostasis and infant health. However, the viral component (known as “virome”) remains mostly unexplored. Here, we establish the Early-Life Gut Virome (ELGV), a catalog of 160,478 non-redundant DNA and RNA viral sequences from 8130 gut virus-like particles (VLPs) enriched or bulk metagenomes in the first three years of life. By clustering, 82,141 viral species are identified, 68.3% of which are absent in existing databases built mainly from adults, and 64 and 8 viral species based on VLPs-enriched and bulk metagenomes, respectively, exhibit potentials as biomarkers to distinguish infants from adults. With the largest longitudinal population of infants profiled by either VLPs-enriched or bulk metagenomic sequencing, we track the inherent instability and temporal development of the early-life human gut virome, and identify differential viruses associated with multiple clinical factors. The mother-infant shared virome and interactions between gut virome and bacteriome early in life are further expanded. Together, the ELGV catalog provides the most comprehensive and complete metagenomic blueprint of the early-life human gut virome, facilitating the discovery of pediatric disease-virome associations in future.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45793-z
    DOI: 10.1038/s41467-024-45793-z
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    as
    1. Himel Mallick & Ali Rahnavard & Lauren J McIver & Siyuan Ma & Yancong Zhang & Long H Nguyen & Timothy L Tickle & George Weingart & Boyu Ren & Emma H Schwager & Suvo Chatterjee & Kelsey N Thompson & Je, 2021. "Multivariable association discovery in population-scale meta-omics studies," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-27, November.
    2. Jai Junbae Jee & Li Yang & Pranavkumar Shivakumar & Pei-pei Xu & Reena Mourya & Unmesha Thanekar & Pu Yu & Yu Zhu & Yongkang Pan & Haibin Wang & Xufei Duan & Yongqin Ye & Bin Wang & Zhu Jin & Yuanmei , 2022. "Maternal regulation of biliary disease in neonates via gut microbial metabolites," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Fiona Fouhy & Claire Watkins & Cian J. Hill & Carol-Anne O’Shea & Brid Nagle & Eugene M. Dempsey & Paul W. O’Toole & R. Paul Ross & C. Anthony Ryan & Catherine Stanton, 2019. "Perinatal factors affect the gut microbiota up to four years after birth," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    4. Ran Li & Yongming Wang & Han Hu & Yan Tan & Yingfei Ma, 2022. "Metagenomic analysis reveals unexplored diversity of archaeal virome in the human gut," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. 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.
    6. Suguru Nishijima & Naoyoshi Nagata & Yuya Kiguchi & Yasushi Kojima & Tohru Miyoshi-Akiyama & Moto Kimura & Mitsuru Ohsugi & Kohjiro Ueki & Shinichi Oka & Masashi Mizokami & Takao Itoi & Takashi Kawai , 2022. "Extensive gut virome variation and its associations with host and environmental factors in a population-level cohort," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    7. 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.
    8. Tommi Vatanen & Eric A. Franzosa & Randall Schwager & Surya Tripathi & Timothy D. Arthur & Kendra Vehik & Åke Lernmark & William A. Hagopian & Marian J. Rewers & Jin-Xiong She & Jorma Toppari & Anette, 2018. "The human gut microbiome in early-onset type 1 diabetes from the TEDDY study," Nature, Nature, vol. 562(7728), pages 589-594, October.
    9. Hothorn, Torsten & Hornik, Kurt & van de Wiel, Mark A. & Zeileis, Achim, 2006. "A Lego System for Conditional Inference," The American Statistician, American Statistical Association, vol. 60, pages 257-263, August.
    10. Shuqin Zeng & Dhrati Patangia & Alexandre Almeida & Zhemin Zhou & Dezhi Mu & R. Paul Ross & Catherine Stanton & Shaopu Wang, 2022. "A compendium of 32,277 metagenome-assembled genomes and over 80 million genes from the early-life human gut microbiome," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Yan Shao & Samuel C. Forster & Evdokia Tsaliki & Kevin Vervier & Angela Strang & Nandi Simpson & Nitin Kumar & Mark D. Stares & Alison Rodger & Peter Brocklehurst & Nigel Field & Trevor D. Lawley, 2019. "Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth," Nature, Nature, vol. 574(7776), pages 117-121, October.
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