Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life

Tommi Vatanen; Damian R. Plichta; Juhi Somani; Philipp C. Münch; Timothy D. Arthur; Andrew Brantley Hall; Sabine Rudolf; Edward J. Oakeley; Xiaobo Ke; Rachel A. Young; Henry J. Haiser; Raivo Kolde; Moran Yassour; Kristiina Luopajärvi; Heli Siljander; Suvi M. Virtanen; Jorma Ilonen; Raivo Uibo; Vallo Tillmann; Sergei Mokurov; Natalya Dorshakova; Jeffrey A. Porter; Alice C. McHardy; Harri Lähdesmäki; Hera Vlamakis; Curtis Huttenhower; Mikael Knip; Ramnik J. Xavier

doi:10.1038/s41564-018-0321-5

Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life

Tommi Vatanen, Damian R. Plichta, Juhi Somani, Philipp C. Münch, Timothy D. Arthur, Andrew Brantley Hall, Sabine Rudolf, Edward J. Oakeley, Xiaobo Ke, Rachel A. Young, Henry J. Haiser, Raivo Kolde, Moran Yassour, Kristiina Luopajärvi, Heli Siljander, Suvi M. Virtanen, Jorma Ilonen, Raivo Uibo, Vallo Tillmann, Sergei MokurovNatalya Dorshakova, Jeffrey A. Porter, Alice C. McHardy, Harri Lähdesmäki, Hera Vlamakis, Curtis Huttenhower, Mikael Knip, Ramnik J. Xavier^*

^*Corresponding author for this work

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

153 Scopus citations

Abstract

The human gut microbiome matures towards the adult composition during the first years of life and is implicated in early immune development. Here, we investigate the effects of microbial genomic diversity on gut microbiome development using integrated early childhood data sets collected in the DIABIMMUNE study in Finland, Estonia and Russian Karelia. We show that gut microbial diversity is associated with household location and linear growth of children. Single nucleotide polymorphism- and metagenomic assembly-based strain tracking revealed large and highly dynamic microbial pangenomes, especially in the genus Bacteroides, in which we identified evidence of variability deriving from Bacteroides-targeting bacteriophages. Our analyses revealed functional consequences of strain diversity; only 10% of Finnish infants harboured Bifidobacterium longum subsp. infantis, a subspecies specialized in human milk metabolism, whereas Russian infants commonly maintained a probiotic Bifidobacterium bifidum strain in infancy. Groups of bacteria contributing to diverse, characterized metabolic pathways converged to highly subject-specific configurations over the first two years of life. This longitudinal study extends the current view of early gut microbial community assembly based on strain-level genomic variation.

Original language	English
Pages (from-to)	470-479
Number of pages	10
Journal	Nature Microbiology
Volume	4
Issue number	3
DOIs	https://doi.org/10.1038/s41564-018-0321-5
State	Published - 1 Mar 2019
Externally published	Yes

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Publisher Copyright:
© 2018, The Author(s), under exclusive licence to Springer Nature Limited.

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Vatanen, T., Plichta, D. R., Somani, J., Münch, P. C., Arthur, T. D., Hall, A. B., Rudolf, S., Oakeley, E. J., Ke, X., Young, R. A., Haiser, H. J., Kolde, R., Yassour, M., Luopajärvi, K., Siljander, H., Virtanen, S. M., Ilonen, J., Uibo, R., Tillmann, V., ... Xavier, R. J. (2019). Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life. Nature Microbiology, 4(3), 470-479. https://doi.org/10.1038/s41564-018-0321-5

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title = "Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life",

abstract = "The human gut microbiome matures towards the adult composition during the first years of life and is implicated in early immune development. Here, we investigate the effects of microbial genomic diversity on gut microbiome development using integrated early childhood data sets collected in the DIABIMMUNE study in Finland, Estonia and Russian Karelia. We show that gut microbial diversity is associated with household location and linear growth of children. Single nucleotide polymorphism- and metagenomic assembly-based strain tracking revealed large and highly dynamic microbial pangenomes, especially in the genus Bacteroides, in which we identified evidence of variability deriving from Bacteroides-targeting bacteriophages. Our analyses revealed functional consequences of strain diversity; only 10% of Finnish infants harboured Bifidobacterium longum subsp. infantis, a subspecies specialized in human milk metabolism, whereas Russian infants commonly maintained a probiotic Bifidobacterium bifidum strain in infancy. Groups of bacteria contributing to diverse, characterized metabolic pathways converged to highly subject-specific configurations over the first two years of life. This longitudinal study extends the current view of early gut microbial community assembly based on strain-level genomic variation.",

author = "Tommi Vatanen and Plichta, {Damian R.} and Juhi Somani and M{\"u}nch, {Philipp C.} and Arthur, {Timothy D.} and Hall, {Andrew Brantley} and Sabine Rudolf and Oakeley, {Edward J.} and Xiaobo Ke and Young, {Rachel A.} and Haiser, {Henry J.} and Raivo Kolde and Moran Yassour and Kristiina Luopaj{\"a}rvi and Heli Siljander and Virtanen, {Suvi M.} and Jorma Ilonen and Raivo Uibo and Vallo Tillmann and Sergei Mokurov and Natalya Dorshakova and Porter, {Jeffrey A.} and McHardy, {Alice C.} and Harri L{\"a}hdesm{\"a}ki and Hera Vlamakis and Curtis Huttenhower and Mikael Knip and Xavier, {Ramnik J.}",

note = "Publisher Copyright: {\textcopyright} 2018, The Author(s), under exclusive licence to Springer Nature Limited.",

year = "2019",

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doi = "10.1038/s41564-018-0321-5",

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Vatanen, T, Plichta, DR, Somani, J, Münch, PC, Arthur, TD, Hall, AB, Rudolf, S, Oakeley, EJ, Ke, X, Young, RA, Haiser, HJ, Kolde, R, Yassour, M, Luopajärvi, K, Siljander, H, Virtanen, SM, Ilonen, J, Uibo, R, Tillmann, V, Mokurov, S, Dorshakova, N, Porter, JA, McHardy, AC, Lähdesmäki, H, Vlamakis, H, Huttenhower, C, Knip, M & Xavier, RJ 2019, 'Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life', Nature Microbiology, vol. 4, no. 3, pp. 470-479. https://doi.org/10.1038/s41564-018-0321-5

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AU - Arthur, Timothy D.

AU - Hall, Andrew Brantley

AU - Rudolf, Sabine

AU - Oakeley, Edward J.

AU - Ke, Xiaobo

AU - Young, Rachel A.

AU - Haiser, Henry J.

AU - Kolde, Raivo

AU - Yassour, Moran

AU - Luopajärvi, Kristiina

AU - Siljander, Heli

AU - Virtanen, Suvi M.

AU - Ilonen, Jorma

AU - Uibo, Raivo

AU - Tillmann, Vallo

AU - Mokurov, Sergei

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AU - Porter, Jeffrey A.

AU - McHardy, Alice C.

AU - Lähdesmäki, Harri

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AU - Knip, Mikael

AU - Xavier, Ramnik J.

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Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life

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