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

Research output: Contribution to journal › Review › Research › peer-review

Standard

Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies. / Kennedy, Katherine M.; de Goffau, Marcus C.; Perez-Muñoz, Maria Elisa; Arrieta, Marie Claire; Bäckhed, Fredrik; Bork, Peer; Braun, Thorsten; Bushman, Frederic D.; Dore, Joel; de Vos, Willem M.; Earl, Ashlee M.; Eisen, Jonathan A.; Elovitz, Michal A.; Ganal-Vonarburg, Stephanie C.; Gänzle, Michael G.; Garrett, Wendy S.; Hall, Lindsay J.; Hornef, Mathias W.; Huttenhower, Curtis; Konnikova, Liza; Lebeer, Sarah; Macpherson, Andrew J.; Massey, Ruth C.; McHardy, Alice Carolyn; Koren, Omry; Lawley, Trevor D.; Ley, Ruth E.; O’Mahony, Liam; O’Toole, Paul W.; Pamer, Eric G.; Parkhill, Julian; Raes, Jeroen; Rattei, Thomas; Salonen, Anne; Segal, Eran; Segata, Nicola; Shanahan, Fergus; Sloboda, Deborah M.; Smith, Gordon C.S.; Sokol, Harry; Spector, Tim D.; Surette, Michael G.; Tannock, Gerald W.; Walker, Alan W.; Yassour, Moran; Walter, Jens.

In: Nature, Vol. 613, No. 7945, 2023, p. 639-649.

Research output: Contribution to journal › Review › Research › peer-review

Harvard

Kennedy, KM, de Goffau, MC, Perez-Muñoz, ME, Arrieta, MC, Bäckhed, F, Bork, P, Braun, T, Bushman, FD, Dore, J, de Vos, WM, Earl, AM, Eisen, JA, Elovitz, MA, Ganal-Vonarburg, SC, Gänzle, MG, Garrett, WS, Hall, LJ, Hornef, MW, Huttenhower, C, Konnikova, L, Lebeer, S, Macpherson, AJ, Massey, RC, McHardy, AC, Koren, O, Lawley, TD, Ley, RE, O’Mahony, L, O’Toole, PW, Pamer, EG, Parkhill, J, Raes, J, Rattei, T, Salonen, A, Segal, E, Segata, N, Shanahan, F, Sloboda, DM, Smith, GCS, Sokol, H, Spector, TD, Surette, MG, Tannock, GW, Walker, AW, Yassour, M & Walter, J 2023, 'Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies', Nature, vol. 613, no. 7945, pp. 639-649. https://doi.org/10.1038/s41586-022-05546-8

APA

Kennedy, K. M., de Goffau, M. C., Perez-Muñoz, M. E., Arrieta, M. C., Bäckhed, F., Bork, P., Braun, T., Bushman, F. D., Dore, J., de Vos, W. M., Earl, A. M., Eisen, J. A., Elovitz, M. A., Ganal-Vonarburg, S. C., Gänzle, M. G., Garrett, W. S., Hall, L. J., Hornef, M. W., Huttenhower, C., ... Walter, J. (2023). Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies. Nature, 613(7945), 639-649. https://doi.org/10.1038/s41586-022-05546-8

Vancouver

Kennedy KM, de Goffau MC, Perez-Muñoz ME, Arrieta MC, Bäckhed F, Bork P et al. Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies. Nature. 2023;613(7945):639-649. https://doi.org/10.1038/s41586-022-05546-8

Author

Kennedy, Katherine M. ; de Goffau, Marcus C. ; Perez-Muñoz, Maria Elisa ; Arrieta, Marie Claire ; Bäckhed, Fredrik ; Bork, Peer ; Braun, Thorsten ; Bushman, Frederic D. ; Dore, Joel ; de Vos, Willem M. ; Earl, Ashlee M. ; Eisen, Jonathan A. ; Elovitz, Michal A. ; Ganal-Vonarburg, Stephanie C. ; Gänzle, Michael G. ; Garrett, Wendy S. ; Hall, Lindsay J. ; Hornef, Mathias W. ; Huttenhower, Curtis ; Konnikova, Liza ; Lebeer, Sarah ; Macpherson, Andrew J. ; Massey, Ruth C. ; McHardy, Alice Carolyn ; Koren, Omry ; Lawley, Trevor D. ; Ley, Ruth E. ; O’Mahony, Liam ; O’Toole, Paul W. ; Pamer, Eric G. ; Parkhill, Julian ; Raes, Jeroen ; Rattei, Thomas ; Salonen, Anne ; Segal, Eran ; Segata, Nicola ; Shanahan, Fergus ; Sloboda, Deborah M. ; Smith, Gordon C.S. ; Sokol, Harry ; Spector, Tim D. ; Surette, Michael G. ; Tannock, Gerald W. ; Walker, Alan W. ; Yassour, Moran ; Walter, Jens. / Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies. In: Nature. 2023 ; Vol. 613, No. 7945. pp. 639-649.

Bibtex

@article{cf81b7aa9cf54246b5153d0ee55af0b0,
title = "Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies",
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.",
author = "Kennedy, {Katherine M.} and {de Goffau}, {Marcus C.} and Perez-Mu{\~n}oz, {Maria Elisa} and Arrieta, {Marie Claire} and Fredrik B{\"a}ckhed and Peer Bork and Thorsten Braun and Bushman, {Frederic D.} and Joel Dore and {de Vos}, {Willem M.} and Earl, {Ashlee M.} and Eisen, {Jonathan A.} and Elovitz, {Michal A.} and Ganal-Vonarburg, {Stephanie C.} and G{\"a}nzle, {Michael G.} and Garrett, {Wendy S.} and Hall, {Lindsay J.} and Hornef, {Mathias W.} and Curtis Huttenhower and Liza Konnikova and Sarah Lebeer and Macpherson, {Andrew J.} and Massey, {Ruth C.} and McHardy, {Alice Carolyn} and Omry Koren and Lawley, {Trevor D.} and Ley, {Ruth E.} and Liam O{\textquoteright}Mahony and O{\textquoteright}Toole, {Paul W.} and Pamer, {Eric G.} and Julian Parkhill and Jeroen Raes and Thomas Rattei and Anne Salonen and Eran Segal and Nicola Segata and Fergus Shanahan and Sloboda, {Deborah M.} and Smith, {Gordon C.S.} and Harry Sokol and Spector, {Tim D.} and Surette, {Michael G.} and Tannock, {Gerald W.} and Walker, {Alan W.} and Moran Yassour and Jens Walter",
note = "Publisher Copyright: {\textcopyright} 2023, Springer Nature Limited.",
year = "2023",
doi = "10.1038/s41586-022-05546-8",
language = "English",
volume = "613",
pages = "639--649",
journal = "Nature",
issn = "0028-0836",
publisher = "nature publishing group",
number = "7945",

}

RIS

TY - JOUR

T1 - Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies

AU - Kennedy, Katherine M.

AU - de Goffau, Marcus C.

AU - Perez-Muñoz, Maria Elisa

AU - Arrieta, Marie Claire

AU - Bäckhed, Fredrik

AU - Bork, Peer

AU - Braun, Thorsten

AU - Bushman, Frederic D.

AU - Dore, Joel

AU - de Vos, Willem M.

AU - Earl, Ashlee M.

AU - Eisen, Jonathan A.

AU - Elovitz, Michal A.

AU - Ganal-Vonarburg, Stephanie C.

AU - Gänzle, Michael G.

AU - Garrett, Wendy S.

AU - Hall, Lindsay J.

AU - Hornef, Mathias W.

AU - Huttenhower, Curtis

AU - Konnikova, Liza

AU - Lebeer, Sarah

AU - Macpherson, Andrew J.

AU - Massey, Ruth C.

AU - McHardy, Alice Carolyn

AU - Koren, Omry

AU - Lawley, Trevor D.

AU - Ley, Ruth E.

AU - O’Mahony, Liam

AU - O’Toole, Paul W.

AU - Pamer, Eric G.

AU - Parkhill, Julian

AU - Raes, Jeroen

AU - Rattei, Thomas

AU - Salonen, Anne

AU - Segal, Eran

AU - Segata, Nicola

AU - Shanahan, Fergus

AU - Sloboda, Deborah M.

AU - Smith, Gordon C.S.

AU - Sokol, Harry

AU - Spector, Tim D.

AU - Surette, Michael G.

AU - Tannock, Gerald W.

AU - Walker, Alan W.

AU - Yassour, Moran

AU - Walter, Jens

N1 - Publisher Copyright: © 2023, Springer Nature Limited.

PY - 2023

Y1 - 2023

N2 - 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.

AB - 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.

U2 - 10.1038/s41586-022-05546-8

DO - 10.1038/s41586-022-05546-8

M3 - Review

C2 - 36697862

AN - SCOPUS:85146875375

VL - 613

SP - 639

EP - 649

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7945

ER -

ID: 336467031