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Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies

Author

Listed:
  • Katherine M. Kennedy

    (McMaster University
    McMaster University)

  • Marcus C. Goffau

    (Tytgat Institute for Liver and Intestinal Research, Amsterdam University Medical Centers
    University of Amsterdam
    Wellcome Sanger Institute)

  • Maria Elisa Perez-Muñoz

    (University of Alberta)

  • Marie-Claire Arrieta

    (University of Calgary)

  • Fredrik Bäckhed

    (University of Gothenburg
    Sahlgrenska University Hospital
    University of Copenhagen)

  • Peer Bork

    (European Molecular Biology Laboratory
    Max Delbrück Centre for Molecular Medicine
    Yonsei University
    University of Würzburg)

  • Thorsten Braun

    (Charité—Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin)

  • Frederic D. Bushman

    (University of Pennsylvania)

  • Joel Dore

    (Université Paris-Saclay, INRAE, MetaGenoPolis, AgroParisTech, MICALIS)

  • Willem M. Vos

    (University of Helsinki
    Wageningen University)

  • Ashlee M. Earl

    (Broad Institute of MIT and Harvard)

  • Jonathan A. Eisen

    (University of California, Davis
    University of California, Davis
    University of California, Davis)

  • Michal A. Elovitz

    (University of Pennsylvania Perelman School of Medicine)

  • Stephanie C. Ganal-Vonarburg

    (Bern University Hospital, University of Bern
    University of Bern)

  • Michael G. Gänzle

    (University of Alberta)

  • Wendy S. Garrett

    (Harvard T.H. Chan School of Public Health
    Harvard T.H. Chan Microbiome in Public Health Center
    Dana-Farber Cancer Institute and Harvard Medical School
    Broad Institute of Harvard and MIT)

  • Lindsay J. Hall

    (Norwich Research Park
    University of East Anglia
    Technical University of Munich)

  • Mathias W. Hornef

    (RWTH University Hospital)

  • Curtis Huttenhower

    (Harvard T.H. Chan School of Public Health
    Broad Institute of Harvard and MIT
    Harvard T.H. Chan School of Public Health)

  • Liza Konnikova

    (Yale School of Medicine)

  • Sarah Lebeer

    (University of Antwerp)

  • Andrew J. Macpherson

    (University of Bern)

  • Ruth C. Massey

    (University College Cork
    University College Cork)

  • Alice Carolyn McHardy

    (Helmholtz Centre for Infection Research
    Hannover Braunschweig site
    Technische Universität Braunschweig)

  • Omry Koren

    (Bar-Ilan University)

  • Trevor D. Lawley

    (University of Amsterdam)

  • Ruth E. Ley

    (Max Planck Institute for Developmental Biology)

  • Liam O’Mahony

    (University College Cork
    University College Cork
    University College Cork)

  • Paul W. O’Toole

    (University College Cork
    University College Cork)

  • Eric G. Pamer

    (University of Chicago)

  • Julian Parkhill

    (University of Cambridge)

  • Jeroen Raes

    (VIB Center for Microbiology
    KU Leuven)

  • Thomas Rattei

    (University of Vienna)

  • Anne Salonen

    (University of Helsinki)

  • Eran Segal

    (Weizmann Institute of Science)

  • Nicola Segata

    (University of Trento
    European Institute of Oncology (IEO), IRCCS)

  • Fergus Shanahan

    (University College Cork
    University College Cork)

  • Deborah M. Sloboda

    (McMaster University
    McMaster University
    McMaster University
    McMaster University)

  • Gordon C. S. Smith

    (University of Cambridge
    NIHR Cambridge Biomedical Research Centre)

  • Harry Sokol

    (AP-HP, Saint Antoine Hospital, Centre de Recherche Saint-Antoine, CRSA, INSERM and Sorbonne Université
    Paris Center for Microbiome Medicine (PaCeMM), Fédération Hospitalo-Universitaire
    Micalis Institute, INRAE, AgroParisTech, Université Paris–Saclay)

  • Tim D. Spector

    (King’s College London)

  • Michael G. Surette

    (McMaster University
    McMaster University
    McMaster University)

  • Gerald W. Tannock

    (University of Otago)

  • Alan W. Walker

    (University of Aberdeen)

  • Moran Yassour

    (The Hebrew University of Jerusalem
    The Hebrew University of Jerusalem)

  • Jens Walter

    (University College Cork
    University College Cork
    University College Cork)

Abstract

Whether the human fetus and the prenatal intrauterine environment (amniotic fluid and placenta) are stably colonized by microbial communities in a healthy pregnancy remains a subject of debate. Here we evaluate recent studies that characterized microbial populations in human fetuses from the perspectives of reproductive biology, microbial ecology, bioinformatics, immunology, clinical microbiology and gnotobiology, and assess possible mechanisms by which the fetus might interact with microorganisms. Our analysis indicates that the detected microbial signals are likely the result of contamination during the clinical procedures to obtain fetal samples or during DNA extraction and DNA sequencing. Furthermore, the existence of live and replicating microbial populations in healthy fetal tissues is not compatible with fundamental concepts of immunology, clinical microbiology and the derivation of germ-free mammals. These conclusions are important to our understanding of human immune development and illustrate common pitfalls in the microbial analyses of many other low-biomass environments. The pursuit of a fetal microbiome serves as a cautionary example of the challenges of sequence-based microbiome studies when biomass is low or absent, and emphasizes the need for a trans-disciplinary approach that goes beyond contamination controls by also incorporating biological, ecological and mechanistic concepts.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:613:y:2023:i:7945:d:10.1038_s41586-022-05546-8
    DOI: 10.1038/s41586-022-05546-8
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    Citations

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    Cited by:

    1. Tomás Clive Barker-Tejeda & Elisa Zubeldia-Varela & Andrea Macías-Camero & Lola Alonso & Isabel Adoración Martín-Antoniano & María Fernanda Rey-Stolle & Leticia Mera-Berriatua & Raphaëlle Bazire & Pau, 2024. "Comparative characterization of the infant gut microbiome and their maternal lineage by a multi-omics approach," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    2. Sivan Kijner & Dena Ennis & Shimrit Shmorak & Anat Florentin & Moran Yassour, 2024. "CRISPR-Cas-based identification of a sialylated human milk oligosaccharides utilization cluster in the infant gut commensal Bacteroides dorei," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Fanette Fontaine & Sondra Turjeman & Karel Callens & Omry Koren, 2023. "The intersection of undernutrition, microbiome, and child development in the first years of life," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    4. 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.

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