Mobile genetic elements from the maternal microbiome shape infant gut microbial assembly and metabolism

Tommi Vatanen; Karolina S. Jabbar; Terhi Ruohtula; Jarno Honkanen; Julian Avila-Pacheco; Heli Siljander; Martin Stražar; Sami Oikarinen; Heikki Hyöty; Jorma Ilonen; Caroline M. Mitchell; Moran Yassour; Suvi M. Virtanen; Clary B. Clish; Damian R. Plichta; Hera Vlamakis; Mikael Knip; Ramnik J. Xavier

doi:10.1016/j.cell.2022.11.023

Mobile genetic elements from the maternal microbiome shape infant gut microbial assembly and metabolism

Tommi Vatanen, Karolina S. Jabbar, Terhi Ruohtula, Jarno Honkanen, Julian Avila-Pacheco, Heli Siljander, Martin Stražar, Sami Oikarinen, Heikki Hyöty, Jorma Ilonen, Caroline M. Mitchell, Moran Yassour, Suvi M. Virtanen, Clary B. Clish, Damian R. Plichta, Hera Vlamakis, Mikael Knip, Ramnik J. Xavier^*

^*Corresponding author for this work

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

54 Scopus citations

Abstract

The perinatal period represents a critical window for cognitive and immune system development, promoted by maternal and infant gut microbiomes and their metabolites. Here, we tracked the co-development of microbiomes and metabolomes from late pregnancy to 1 year of age using longitudinal multi-omics data from a cohort of 70 mother-infant dyads. We discovered large-scale mother-to-infant interspecies transfer of mobile genetic elements, frequently involving genes associated with diet-related adaptations. Infant gut metabolomes were less diverse than maternal but featured hundreds of unique metabolites and microbe-metabolite associations not detected in mothers. Metabolomes and serum cytokine signatures of infants who received regular—but not extensively hydrolyzed—formula were distinct from those of exclusively breastfed infants. Taken together, our integrative analysis expands the concept of vertical transmission of the gut microbiome and provides original insights into the development of maternal and infant microbiomes and metabolomes during late pregnancy and early life.

Original language	English
Pages (from-to)	4921-4936.e15
Journal	Cell
Volume	185
Issue number	26
DOIs	https://doi.org/10.1016/j.cell.2022.11.023
State	Published - 22 Dec 2022

Bibliographical note

Publisher Copyright:
© 2022 Elsevier Inc.

Keywords

gut metabolome
horizontal gene transfer
infant gut microbiome
mother-to-infant microbiome transmission

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10.1016/j.cell.2022.11.023

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Vatanen, T., Jabbar, K. S., Ruohtula, T., Honkanen, J., Avila-Pacheco, J., Siljander, H., Stražar, M., Oikarinen, S., Hyöty, H., Ilonen, J., Mitchell, C. M., Yassour, M., Virtanen, S. M., Clish, C. B., Plichta, D. R., Vlamakis, H., Knip, M., & Xavier, R. J. (2022). Mobile genetic elements from the maternal microbiome shape infant gut microbial assembly and metabolism. Cell, 185(26), 4921-4936.e15. https://doi.org/10.1016/j.cell.2022.11.023

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abstract = "The perinatal period represents a critical window for cognitive and immune system development, promoted by maternal and infant gut microbiomes and their metabolites. Here, we tracked the co-development of microbiomes and metabolomes from late pregnancy to 1 year of age using longitudinal multi-omics data from a cohort of 70 mother-infant dyads. We discovered large-scale mother-to-infant interspecies transfer of mobile genetic elements, frequently involving genes associated with diet-related adaptations. Infant gut metabolomes were less diverse than maternal but featured hundreds of unique metabolites and microbe-metabolite associations not detected in mothers. Metabolomes and serum cytokine signatures of infants who received regular—but not extensively hydrolyzed—formula were distinct from those of exclusively breastfed infants. Taken together, our integrative analysis expands the concept of vertical transmission of the gut microbiome and provides original insights into the development of maternal and infant microbiomes and metabolomes during late pregnancy and early life.",

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Vatanen, T, Jabbar, KS, Ruohtula, T, Honkanen, J, Avila-Pacheco, J, Siljander, H, Stražar, M, Oikarinen, S, Hyöty, H, Ilonen, J, Mitchell, CM, Yassour, M, Virtanen, SM, Clish, CB, Plichta, DR, Vlamakis, H, Knip, M & Xavier, RJ 2022, 'Mobile genetic elements from the maternal microbiome shape infant gut microbial assembly and metabolism', Cell, vol. 185, no. 26, pp. 4921-4936.e15. https://doi.org/10.1016/j.cell.2022.11.023

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AU - Jabbar, Karolina S.

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AU - Stražar, Martin

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AU - Yassour, Moran

AU - Virtanen, Suvi M.

AU - Clish, Clary B.

AU - Plichta, Damian R.

AU - Vlamakis, Hera

AU - Knip, Mikael

AU - Xavier, Ramnik J.

PY - 2022/12/22

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N2 - The perinatal period represents a critical window for cognitive and immune system development, promoted by maternal and infant gut microbiomes and their metabolites. Here, we tracked the co-development of microbiomes and metabolomes from late pregnancy to 1 year of age using longitudinal multi-omics data from a cohort of 70 mother-infant dyads. We discovered large-scale mother-to-infant interspecies transfer of mobile genetic elements, frequently involving genes associated with diet-related adaptations. Infant gut metabolomes were less diverse than maternal but featured hundreds of unique metabolites and microbe-metabolite associations not detected in mothers. Metabolomes and serum cytokine signatures of infants who received regular—but not extensively hydrolyzed—formula were distinct from those of exclusively breastfed infants. Taken together, our integrative analysis expands the concept of vertical transmission of the gut microbiome and provides original insights into the development of maternal and infant microbiomes and metabolomes during late pregnancy and early life.

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Mobile genetic elements from the maternal microbiome shape infant gut microbial assembly and metabolism

Abstract

Bibliographical note

Keywords

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