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Selective maternal seeding and environment shape the human gut microbiome

Vertical transmission of bacteria from mother to infant at birth is postulated to initiate a life-long host-microbe symbiosis, playing an important role in early infant development. However, only the tracking of strictly defined unique microbial strains can clarify where the intestinal bacteria come...

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Autores principales: Korpela, Katri, Costea, Paul, Coelho, Luis Pedro, Kandels-Lewis, Stefanie, Willemsen, Gonneke, Boomsma, Dorret I., Segata, Nicola, Bork, Peer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880245/
https://www.ncbi.nlm.nih.gov/pubmed/29496731
http://dx.doi.org/10.1101/gr.233940.117
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author Korpela, Katri
Costea, Paul
Coelho, Luis Pedro
Kandels-Lewis, Stefanie
Willemsen, Gonneke
Boomsma, Dorret I.
Segata, Nicola
Bork, Peer
author_facet Korpela, Katri
Costea, Paul
Coelho, Luis Pedro
Kandels-Lewis, Stefanie
Willemsen, Gonneke
Boomsma, Dorret I.
Segata, Nicola
Bork, Peer
author_sort Korpela, Katri
collection PubMed
description Vertical transmission of bacteria from mother to infant at birth is postulated to initiate a life-long host-microbe symbiosis, playing an important role in early infant development. However, only the tracking of strictly defined unique microbial strains can clarify where the intestinal bacteria come from, how long the initial colonizers persist, and whether colonization by other strains from the environment can replace existing ones. Using rare single nucleotide variants in fecal metagenomes of infants and their family members, we show strong evidence of selective and persistent transmission of maternal strain populations to the vaginally born infant and their occasional replacement by strains from the environment, including those from family members, in later childhood. Only strains from the classes Actinobacteria and Bacteroidia, which are essential components of the infant microbiome, are transmitted from the mother and persist for at least 1 yr. In contrast, maternal strains of Clostridia, a dominant class in the mother's gut microbiome, are not observed in the infant. Caesarean-born infants show a striking lack of maternal transmission at birth. After the first year, strain influx from the family environment occurs and continues even in adulthood. Fathers appear to be more frequently donors of novel strains to other family members than receivers. Thus, the infant gut is seeded by selected maternal bacteria, which expand to form a stable community, with a rare but stable continuing strain influx over time.
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spelling pubmed-58802452018-04-13 Selective maternal seeding and environment shape the human gut microbiome Korpela, Katri Costea, Paul Coelho, Luis Pedro Kandels-Lewis, Stefanie Willemsen, Gonneke Boomsma, Dorret I. Segata, Nicola Bork, Peer Genome Res Research Vertical transmission of bacteria from mother to infant at birth is postulated to initiate a life-long host-microbe symbiosis, playing an important role in early infant development. However, only the tracking of strictly defined unique microbial strains can clarify where the intestinal bacteria come from, how long the initial colonizers persist, and whether colonization by other strains from the environment can replace existing ones. Using rare single nucleotide variants in fecal metagenomes of infants and their family members, we show strong evidence of selective and persistent transmission of maternal strain populations to the vaginally born infant and their occasional replacement by strains from the environment, including those from family members, in later childhood. Only strains from the classes Actinobacteria and Bacteroidia, which are essential components of the infant microbiome, are transmitted from the mother and persist for at least 1 yr. In contrast, maternal strains of Clostridia, a dominant class in the mother's gut microbiome, are not observed in the infant. Caesarean-born infants show a striking lack of maternal transmission at birth. After the first year, strain influx from the family environment occurs and continues even in adulthood. Fathers appear to be more frequently donors of novel strains to other family members than receivers. Thus, the infant gut is seeded by selected maternal bacteria, which expand to form a stable community, with a rare but stable continuing strain influx over time. Cold Spring Harbor Laboratory Press 2018-04 /pmc/articles/PMC5880245/ /pubmed/29496731 http://dx.doi.org/10.1101/gr.233940.117 Text en © 2018 Korpela et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by/4.0/ This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research
Korpela, Katri
Costea, Paul
Coelho, Luis Pedro
Kandels-Lewis, Stefanie
Willemsen, Gonneke
Boomsma, Dorret I.
Segata, Nicola
Bork, Peer
Selective maternal seeding and environment shape the human gut microbiome
title Selective maternal seeding and environment shape the human gut microbiome
title_full Selective maternal seeding and environment shape the human gut microbiome
title_fullStr Selective maternal seeding and environment shape the human gut microbiome
title_full_unstemmed Selective maternal seeding and environment shape the human gut microbiome
title_short Selective maternal seeding and environment shape the human gut microbiome
title_sort selective maternal seeding and environment shape the human gut microbiome
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880245/
https://www.ncbi.nlm.nih.gov/pubmed/29496731
http://dx.doi.org/10.1101/gr.233940.117
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