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

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 DIABI...

Full description

Bibliographic Details
Published in:Nature Microbiology
Main Authors: Vatanen, Tommi, Plichta, Damian R., Somani, Juhi, Muench, Philipp C., Arthur, Timothy D., Hall, Andrew Brantley, Rudolf, Sabine, Oakeley, Edward J., Ke, Xiaobo, Young, Rachel A., Haiser, Henry J., Kolde, Raivo, Yassour, Moran, Luopajärvi, Kristiina, Siljander, Heli, Virtanen, Suvi M., Ilonen, Jorma, Uibo, Raivo, Tillmann, Vallo, Mokurov, Sergei, Dorshakova, Natalya, Porter, Jeffrey A., McHardy, Alice C., Lahdesmaki, Harri, Vlamakis, Hera, Huttenhower, Curtis, Knip, Mikael, Xavier, Ramnik J.
Other Authors: HUS Children and Adolescents, Diabetes and Obesity Research Program, Children's Hospital, Research Programs Unit, Lastentautien yksikkö, Clinicum, Mikael Knip / Principal Investigator
Format: Article in Journal/Newspaper
Language:English
Published: Nature Publishing Group 2020
Subjects:
Online Access:http://hdl.handle.net/10138/313088
id ftunivhelsihelda:oai:helda.helsinki.fi:10138/313088
record_format openpolar
institution Open Polar
collection HELDA – University of Helsinki Open Repository
op_collection_id ftunivhelsihelda
language English
topic BACTERIAL TRANSMISSION
READ ALIGNMENT
BODY SITES
AUTOIMMUNITY
DYNAMICS
ACCURATE
REVEALS
BIFIDOBACTERIA
ASSOCIATION
INSIGHTS
3111 Biomedicine
1183 Plant biology
microbiology
virology
3123 Gynaecology and paediatrics
spellingShingle BACTERIAL TRANSMISSION
READ ALIGNMENT
BODY SITES
AUTOIMMUNITY
DYNAMICS
ACCURATE
REVEALS
BIFIDOBACTERIA
ASSOCIATION
INSIGHTS
3111 Biomedicine
1183 Plant biology
microbiology
virology
3123 Gynaecology and paediatrics
Vatanen, Tommi
Plichta, Damian R.
Somani, Juhi
Muench, Philipp C.
Arthur, Timothy D.
Hall, Andrew Brantley
Rudolf, Sabine
Oakeley, Edward J.
Ke, Xiaobo
Young, Rachel A.
Haiser, Henry J.
Kolde, Raivo
Yassour, Moran
Luopajärvi, Kristiina
Siljander, Heli
Virtanen, Suvi M.
Ilonen, Jorma
Uibo, Raivo
Tillmann, Vallo
Mokurov, Sergei
Dorshakova, Natalya
Porter, Jeffrey A.
McHardy, Alice C.
Lahdesmaki, Harri
Vlamakis, Hera
Huttenhower, Curtis
Knip, Mikael
Xavier, Ramnik J.
Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life
topic_facet BACTERIAL TRANSMISSION
READ ALIGNMENT
BODY SITES
AUTOIMMUNITY
DYNAMICS
ACCURATE
REVEALS
BIFIDOBACTERIA
ASSOCIATION
INSIGHTS
3111 Biomedicine
1183 Plant biology
microbiology
virology
3123 Gynaecology and paediatrics
description 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. Peer reviewed
author2 HUS Children and Adolescents
Diabetes and Obesity Research Program
Children's Hospital
Research Programs Unit
Lastentautien yksikkö
Clinicum
Mikael Knip / Principal Investigator
format Article in Journal/Newspaper
author Vatanen, Tommi
Plichta, Damian R.
Somani, Juhi
Muench, Philipp C.
Arthur, Timothy D.
Hall, Andrew Brantley
Rudolf, Sabine
Oakeley, Edward J.
Ke, Xiaobo
Young, Rachel A.
Haiser, Henry J.
Kolde, Raivo
Yassour, Moran
Luopajärvi, Kristiina
Siljander, Heli
Virtanen, Suvi M.
Ilonen, Jorma
Uibo, Raivo
Tillmann, Vallo
Mokurov, Sergei
Dorshakova, Natalya
Porter, Jeffrey A.
McHardy, Alice C.
Lahdesmaki, Harri
Vlamakis, Hera
Huttenhower, Curtis
Knip, Mikael
Xavier, Ramnik J.
author_facet Vatanen, Tommi
Plichta, Damian R.
Somani, Juhi
Muench, Philipp C.
Arthur, Timothy D.
Hall, Andrew Brantley
Rudolf, Sabine
Oakeley, Edward J.
Ke, Xiaobo
Young, Rachel A.
Haiser, Henry J.
Kolde, Raivo
Yassour, Moran
Luopajärvi, Kristiina
Siljander, Heli
Virtanen, Suvi M.
Ilonen, Jorma
Uibo, Raivo
Tillmann, Vallo
Mokurov, Sergei
Dorshakova, Natalya
Porter, Jeffrey A.
McHardy, Alice C.
Lahdesmaki, Harri
Vlamakis, Hera
Huttenhower, Curtis
Knip, Mikael
Xavier, Ramnik J.
author_sort Vatanen, Tommi
title Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life
title_short Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life
title_full Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life
title_fullStr Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life
title_full_unstemmed Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life
title_sort genomic variation and strain-specific functional adaptation in the human gut microbiome during early life
publisher Nature Publishing Group
publishDate 2020
url http://hdl.handle.net/10138/313088
genre karelia*
genre_facet karelia*
op_relation 10.1038/s41564-018-0321-5
The authors thank T. Poon and S. Steelman (Broad Institute) for help with sequence production and sample management, A. Rahnavard for help with HMP SNP haplotype analysis, D. Shungin for discussions and connections regarding the use of infant milk products in Russia, K. Koski and M. Koski (University of Helsinki) for the coordination and database work in the DIABIMMUNE study and T. Reimels for editorial help with writing and figure generation. T.V. was supported by funding from the Juvenile Diabetes Research Foundation (JDRF). A.B.H. is a Merck Fellow of the Helen Hay Whitney Foundation. P.C.M. received funding from the German Research Foundation (grant no. 315980449). C.H. was supported by funding from the JDRF (3-SRA-2016-141-Q-R) and the National Institutes of Health (R24DK110499). M. K. was supported by the European Union Seventh Framework Programme FP7/2007-2013 (202063) and the Academy of Finland Centre of Excellence in Molecular Systems Immunology and Physiology Research (250114). R.J.X. was supported by funding from JDRF (2-SRA-2016-247-S-B and 2-SRA-2018-548-S-B), the National Institutes of Health (DK43351 and AI110498) and the Center for Microbiome Informatics and Therapeutics.
Vatanen , T , Plichta , D R , Somani , J , Muench , 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 , Mokurov , S , Dorshakova , N , Porter , J A , McHardy , A C , Lahdesmaki , H , Vlamakis , H , Huttenhower , C , Knip , M & Xavier , R J 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
ORCID: /0000-0002-9428-1282/work/55062303
ORCID: /0000-0003-0949-1291/work/127510071
85058838977
0df0072b-e775-43f7-b243-211267bb4da2
http://hdl.handle.net/10138/313088
000459201400016
op_rights unspecified
openAccess
info:eu-repo/semantics/openAccess
container_title Nature Microbiology
container_volume 4
container_issue 3
container_start_page 470
op_container_end_page 479
_version_ 1787425896858124288
spelling ftunivhelsihelda:oai:helda.helsinki.fi:10138/313088 2024-01-07T09:44:30+01:00 Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life Vatanen, Tommi Plichta, Damian R. Somani, Juhi Muench, Philipp C. Arthur, Timothy D. Hall, Andrew Brantley Rudolf, Sabine Oakeley, Edward J. Ke, Xiaobo Young, Rachel A. Haiser, Henry J. Kolde, Raivo Yassour, Moran Luopajärvi, Kristiina Siljander, Heli Virtanen, Suvi M. Ilonen, Jorma Uibo, Raivo Tillmann, Vallo Mokurov, Sergei Dorshakova, Natalya Porter, Jeffrey A. McHardy, Alice C. Lahdesmaki, Harri Vlamakis, Hera Huttenhower, Curtis Knip, Mikael Xavier, Ramnik J. HUS Children and Adolescents Diabetes and Obesity Research Program Children's Hospital Research Programs Unit Lastentautien yksikkö Clinicum Mikael Knip / Principal Investigator 2020-03-07T23:46:50Z 10 application/pdf http://hdl.handle.net/10138/313088 eng eng Nature Publishing Group 10.1038/s41564-018-0321-5 The authors thank T. Poon and S. Steelman (Broad Institute) for help with sequence production and sample management, A. Rahnavard for help with HMP SNP haplotype analysis, D. Shungin for discussions and connections regarding the use of infant milk products in Russia, K. Koski and M. Koski (University of Helsinki) for the coordination and database work in the DIABIMMUNE study and T. Reimels for editorial help with writing and figure generation. T.V. was supported by funding from the Juvenile Diabetes Research Foundation (JDRF). A.B.H. is a Merck Fellow of the Helen Hay Whitney Foundation. P.C.M. received funding from the German Research Foundation (grant no. 315980449). C.H. was supported by funding from the JDRF (3-SRA-2016-141-Q-R) and the National Institutes of Health (R24DK110499). M. K. was supported by the European Union Seventh Framework Programme FP7/2007-2013 (202063) and the Academy of Finland Centre of Excellence in Molecular Systems Immunology and Physiology Research (250114). R.J.X. was supported by funding from JDRF (2-SRA-2016-247-S-B and 2-SRA-2018-548-S-B), the National Institutes of Health (DK43351 and AI110498) and the Center for Microbiome Informatics and Therapeutics. Vatanen , T , Plichta , D R , Somani , J , Muench , 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 , Mokurov , S , Dorshakova , N , Porter , J A , McHardy , A C , Lahdesmaki , H , Vlamakis , H , Huttenhower , C , Knip , M & Xavier , R J 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 ORCID: /0000-0002-9428-1282/work/55062303 ORCID: /0000-0003-0949-1291/work/127510071 85058838977 0df0072b-e775-43f7-b243-211267bb4da2 http://hdl.handle.net/10138/313088 000459201400016 unspecified openAccess info:eu-repo/semantics/openAccess BACTERIAL TRANSMISSION READ ALIGNMENT BODY SITES AUTOIMMUNITY DYNAMICS ACCURATE REVEALS BIFIDOBACTERIA ASSOCIATION INSIGHTS 3111 Biomedicine 1183 Plant biology microbiology virology 3123 Gynaecology and paediatrics Article publishedVersion 2020 ftunivhelsihelda 2023-12-14T00:13:12Z 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. Peer reviewed Article in Journal/Newspaper karelia* HELDA – University of Helsinki Open Repository Nature Microbiology 4 3 470 479