Successional Stages in Infant Gut Microbiota Maturation
After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors. Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been assoc...
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Published in | mBio Vol. 12; no. 6; p. e0185721 |
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Main Authors | , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
American Society for Microbiology
21.12.2021
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Subjects | |
Online Access | Get full text |
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Abstract | After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors.
Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host conditions. Although early-life factors have been shown to affect infant gut microbiota development, our current understanding of human gut colonization in early life remains limited. To gain more insights into the unique dynamics of this rapidly evolving ecosystem, we investigated the microbiota over the first year of life in eight densely sampled infants (
n
= 303 total samples). To evaluate the gut microbiota maturation transition toward an adult configuration, we compared the microbiome composition of the infants to that of the Flemish Gut Flora Project (FGFP) population (
n
= 1,106). We observed the infant gut microbiota to mature through three distinct, conserved stages of ecosystem development. Across these successional gut microbiota maturation stages, the genus predominance was observed to shift from
Escherichia
over
Bifidobacterium
to
Bacteroides
. Both disease and antibiotic treatment were observed to be associated occasionally with gut microbiota maturation stage regression, a transient setback in microbiota maturation dynamics. Although the studied microbiota trajectories evolved to more adult-like constellations, microbiome community typing against the background of the FGFP cohort clustered all infant samples within the (in adults) potentially dysbiotic
Bacteroides
2 (Bact2) enterotype. We confirmed the similarities between infant gut microbial colonization and adult dysbiosis. Profound knowledge about the primary gut colonization process in infants might provide crucial insights into how the secondary colonization of a dysbiotic adult gut can be redirected.
IMPORTANCE
After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors. Studying this process in detail requires a dense longitudinal sampling effort. In the current study, the bacterial microbiota of >300 stool samples was analyzed from 8 healthy infants, suggesting that the infant gut microbial population matures along a path involving distinct microbial constellations and that the timing of these transitions is infant specific and can temporarily retrace upon external events. We also showed that the infant microbial populations show similarities to suboptimal bacterial populations in the guts of adults. These insights are crucial for a better understanding of the dynamics and characteristics of a “healthy gut microbial population” in both infants and adults and might allow the identification of intervention targets in cases of microbial disturbances or disease. |
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AbstractList | After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors.
Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host conditions. Although early-life factors have been shown to affect infant gut microbiota development, our current understanding of human gut colonization in early life remains limited. To gain more insights into the unique dynamics of this rapidly evolving ecosystem, we investigated the microbiota over the first year of life in eight densely sampled infants (
n
= 303 total samples). To evaluate the gut microbiota maturation transition toward an adult configuration, we compared the microbiome composition of the infants to that of the Flemish Gut Flora Project (FGFP) population (
n
= 1,106). We observed the infant gut microbiota to mature through three distinct, conserved stages of ecosystem development. Across these successional gut microbiota maturation stages, the genus predominance was observed to shift from
Escherichia
over
Bifidobacterium
to
Bacteroides
. Both disease and antibiotic treatment were observed to be associated occasionally with gut microbiota maturation stage regression, a transient setback in microbiota maturation dynamics. Although the studied microbiota trajectories evolved to more adult-like constellations, microbiome community typing against the background of the FGFP cohort clustered all infant samples within the (in adults) potentially dysbiotic
Bacteroides
2 (Bact2) enterotype. We confirmed the similarities between infant gut microbial colonization and adult dysbiosis. Profound knowledge about the primary gut colonization process in infants might provide crucial insights into how the secondary colonization of a dysbiotic adult gut can be redirected.
IMPORTANCE
After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors. Studying this process in detail requires a dense longitudinal sampling effort. In the current study, the bacterial microbiota of >300 stool samples was analyzed from 8 healthy infants, suggesting that the infant gut microbial population matures along a path involving distinct microbial constellations and that the timing of these transitions is infant specific and can temporarily retrace upon external events. We also showed that the infant microbial populations show similarities to suboptimal bacterial populations in the guts of adults. These insights are crucial for a better understanding of the dynamics and characteristics of a “healthy gut microbial population” in both infants and adults and might allow the identification of intervention targets in cases of microbial disturbances or disease. Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host conditions. Although early-life factors have been shown to affect infant gut microbiota development, our current understanding of human gut colonization in early life remains limited. To gain more insights into the unique dynamics of this rapidly evolving ecosystem, we investigated the microbiota over the first year of life in eight densely sampled infants ( = 303 total samples). To evaluate the gut microbiota maturation transition toward an adult configuration, we compared the microbiome composition of the infants to that of the Flemish Gut Flora Project (FGFP) population ( = 1,106). We observed the infant gut microbiota to mature through three distinct, conserved stages of ecosystem development. Across these successional gut microbiota maturation stages, the genus predominance was observed to shift from Escherichia over to . Both disease and antibiotic treatment were observed to be associated occasionally with gut microbiota maturation stage regression, a transient setback in microbiota maturation dynamics. Although the studied microbiota trajectories evolved to more adult-like constellations, microbiome community typing against the background of the FGFP cohort clustered all infant samples within the (in adults) potentially dysbiotic 2 (Bact2) enterotype. We confirmed the similarities between infant gut microbial colonization and adult dysbiosis. Profound knowledge about the primary gut colonization process in infants might provide crucial insights into how the secondary colonization of a dysbiotic adult gut can be redirected. After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors. Studying this process in detail requires a dense longitudinal sampling effort. In the current study, the bacterial microbiota of >300 stool samples was analyzed from 8 healthy infants, suggesting that the infant gut microbial population matures along a path involving distinct microbial constellations and that the timing of these transitions is infant specific and can temporarily retrace upon external events. We also showed that the infant microbial populations show similarities to suboptimal bacterial populations in the guts of adults. These insights are crucial for a better understanding of the dynamics and characteristics of a "healthy gut microbial population" in both infants and adults and might allow the identification of intervention targets in cases of microbial disturbances or disease. Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host conditions. Although early-life factors have been shown to affect infant gut microbiota development, our current understanding of human gut colonization in early life remains limited. To gain more insights into the unique dynamics of this rapidly evolving ecosystem, we investigated the microbiota over the first year of life in eight densely sampled infants (n = 303 total samples). To evaluate the gut microbiota maturation transition toward an adult configuration, we compared the microbiome composition of the infants to that of the Flemish Gut Flora Project (FGFP) population (n = 1,106). We observed the infant gut microbiota to mature through three distinct, conserved stages of ecosystem development. Across these successional gut microbiota maturation stages, the genus predominance was observed to shift from Escherichia over Bifidobacterium to Bacteroides. Both disease and antibiotic treatment were observed to be associated occasionally with gut microbiota maturation stage regression, a transient setback in microbiota maturation dynamics. Although the studied microbiota trajectories evolved to more adult-like constellations, microbiome community typing against the background of the FGFP cohort clustered all infant samples within the (in adults) potentially dysbiotic Bacteroides 2 (Bact2) enterotype. We confirmed the similarities between infant gut microbial colonization and adult dysbiosis. Profound knowledge about the primary gut colonization process in infants might provide crucial insights into how the secondary colonization of a dysbiotic adult gut can be redirected. IMPORTANCE After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors. Studying this process in detail requires a dense longitudinal sampling effort. In the current study, the bacterial microbiota of >300 stool samples was analyzed from 8 healthy infants, suggesting that the infant gut microbial population matures along a path involving distinct microbial constellations and that the timing of these transitions is infant specific and can temporarily retrace upon external events. We also showed that the infant microbial populations show similarities to suboptimal bacterial populations in the guts of adults. These insights are crucial for a better understanding of the dynamics and characteristics of a "healthy gut microbial population" in both infants and adults and might allow the identification of intervention targets in cases of microbial disturbances or disease.Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host conditions. Although early-life factors have been shown to affect infant gut microbiota development, our current understanding of human gut colonization in early life remains limited. To gain more insights into the unique dynamics of this rapidly evolving ecosystem, we investigated the microbiota over the first year of life in eight densely sampled infants (n = 303 total samples). To evaluate the gut microbiota maturation transition toward an adult configuration, we compared the microbiome composition of the infants to that of the Flemish Gut Flora Project (FGFP) population (n = 1,106). We observed the infant gut microbiota to mature through three distinct, conserved stages of ecosystem development. Across these successional gut microbiota maturation stages, the genus predominance was observed to shift from Escherichia over Bifidobacterium to Bacteroides. Both disease and antibiotic treatment were observed to be associated occasionally with gut microbiota maturation stage regression, a transient setback in microbiota maturation dynamics. Although the studied microbiota trajectories evolved to more adult-like constellations, microbiome community typing against the background of the FGFP cohort clustered all infant samples within the (in adults) potentially dysbiotic Bacteroides 2 (Bact2) enterotype. We confirmed the similarities between infant gut microbial colonization and adult dysbiosis. Profound knowledge about the primary gut colonization process in infants might provide crucial insights into how the secondary colonization of a dysbiotic adult gut can be redirected. IMPORTANCE After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors. Studying this process in detail requires a dense longitudinal sampling effort. In the current study, the bacterial microbiota of >300 stool samples was analyzed from 8 healthy infants, suggesting that the infant gut microbial population matures along a path involving distinct microbial constellations and that the timing of these transitions is infant specific and can temporarily retrace upon external events. We also showed that the infant microbial populations show similarities to suboptimal bacterial populations in the guts of adults. These insights are crucial for a better understanding of the dynamics and characteristics of a "healthy gut microbial population" in both infants and adults and might allow the identification of intervention targets in cases of microbial disturbances or disease. Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host conditions. Although early-life factors have been shown to affect infant gut microbiota development, our current understanding of human gut colonization in early life remains limited. To gain more insights into the unique dynamics of this rapidly evolving ecosystem, we investigated the microbiota over the first year of life in eight densely sampled infants (n = 303 total samples). To evaluate the gut microbiota maturation transition toward an adult configuration, we compared the microbiome composition of the infants to that of the Flemish Gut Flora Project (FGFP) population (n = 1,106). We observed the infant gut microbiota to mature through three distinct, conserved stages of ecosystem development. Across these successional gut microbiota maturation stages, the genus predominance was observed to shift from Escherichia over Bifidobacterium to Bacteroides. Both disease and antibiotic treatment were observed to be associated occasionally with gut microbiota maturation stage regression, a transient setback in microbiota maturation dynamics. Although the studied microbiota trajectories evolved to more adult-like constellations, microbiome community typing against the background of the FGFP cohort clustered all infant samples within the (in adults) potentially dysbiotic Bacteroides 2 (Bact2) enterotype. We confirmed the similarities between infant gut microbial colonization and adult dysbiosis. Profound knowledge about the primary gut colonization process in infants might provide crucial insights into how the secondary colonization of a dysbiotic adult gut can be redirected. IMPORTANCE After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors. Studying this process in detail requires a dense longitudinal sampling effort. In the current study, the bacterial microbiota of >300 stool samples was analyzed from 8 healthy infants, suggesting that the infant gut microbial population matures along a path involving distinct microbial constellations and that the timing of these transitions is infant specific and can temporarily retrace upon external events. We also showed that the infant microbial populations show similarities to suboptimal bacterial populations in the guts of adults. These insights are crucial for a better understanding of the dynamics and characteristics of a “healthy gut microbial population” in both infants and adults and might allow the identification of intervention targets in cases of microbial disturbances or disease. Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host conditions. Although early-life factors have been shown to affect infant gut microbiota development, our current understanding of human gut colonization in early life remains limited. To gain more insights into the unique dynamics of this rapidly evolving ecosystem, we investigated the microbiota over the first year of life in eight densely sampled infants ( n = 303 total samples). To evaluate the gut microbiota maturation transition toward an adult configuration, we compared the microbiome composition of the infants to that of the Flemish Gut Flora Project (FGFP) population ( n = 1,106). We observed the infant gut microbiota to mature through three distinct, conserved stages of ecosystem development. Across these successional gut microbiota maturation stages, the genus predominance was observed to shift from Escherichia over Bifidobacterium to Bacteroides . Both disease and antibiotic treatment were observed to be associated occasionally with gut microbiota maturation stage regression, a transient setback in microbiota maturation dynamics. Although the studied microbiota trajectories evolved to more adult-like constellations, microbiome community typing against the background of the FGFP cohort clustered all infant samples within the (in adults) potentially dysbiotic Bacteroides 2 (Bact2) enterotype. We confirmed the similarities between infant gut microbial colonization and adult dysbiosis. Profound knowledge about the primary gut colonization process in infants might provide crucial insights into how the secondary colonization of a dysbiotic adult gut can be redirected. ABSTRACT Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host conditions. Although early-life factors have been shown to affect infant gut microbiota development, our current understanding of human gut colonization in early life remains limited. To gain more insights into the unique dynamics of this rapidly evolving ecosystem, we investigated the microbiota over the first year of life in eight densely sampled infants (n = 303 total samples). To evaluate the gut microbiota maturation transition toward an adult configuration, we compared the microbiome composition of the infants to that of the Flemish Gut Flora Project (FGFP) population (n = 1,106). We observed the infant gut microbiota to mature through three distinct, conserved stages of ecosystem development. Across these successional gut microbiota maturation stages, the genus predominance was observed to shift from Escherichia over Bifidobacterium to Bacteroides. Both disease and antibiotic treatment were observed to be associated occasionally with gut microbiota maturation stage regression, a transient setback in microbiota maturation dynamics. Although the studied microbiota trajectories evolved to more adult-like constellations, microbiome community typing against the background of the FGFP cohort clustered all infant samples within the (in adults) potentially dysbiotic Bacteroides 2 (Bact2) enterotype. We confirmed the similarities between infant gut microbial colonization and adult dysbiosis. Profound knowledge about the primary gut colonization process in infants might provide crucial insights into how the secondary colonization of a dysbiotic adult gut can be redirected. IMPORTANCE After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and influenced by many factors. Studying this process in detail requires a dense longitudinal sampling effort. In the current study, the bacterial microbiota of >300 stool samples was analyzed from 8 healthy infants, suggesting that the infant gut microbial population matures along a path involving distinct microbial constellations and that the timing of these transitions is infant specific and can temporarily retrace upon external events. We also showed that the infant microbial populations show similarities to suboptimal bacterial populations in the guts of adults. These insights are crucial for a better understanding of the dynamics and characteristics of a “healthy gut microbial population” in both infants and adults and might allow the identification of intervention targets in cases of microbial disturbances or disease. |
Author | Falony, Gwen Faust, Karoline Van Ranst, Marc Jansen, Daan Van Espen, Lore Vieira-Silva, Sara Valles-Colomer, Mireia Rymenans, Leen Yinda, Claude Kwe Matthijnssens, Jelle Shi, Chenyan Tito, Raul Yhossef Deboutte, Ward Zeller, Mark Beller, Leen Papadaki, Maria Ioanna Raes, Jeroen |
Author_xml | – sequence: 1 givenname: Leen surname: Beller fullname: Beller, Leen organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Viral Metagenomics, Leuven, Belgium – sequence: 2 givenname: Ward orcidid: 0000-0002-3829-1056 surname: Deboutte fullname: Deboutte, Ward organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Viral Metagenomics, Leuven, Belgium – sequence: 3 givenname: Gwen surname: Falony fullname: Falony, Gwen organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Molecular Bacteriology, Leuven, Belgium, Center for Microbiology, VIB, Leuven, Belgium – sequence: 4 givenname: Sara surname: Vieira-Silva fullname: Vieira-Silva, Sara organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Molecular Bacteriology, Leuven, Belgium, Center for Microbiology, VIB, Leuven, Belgium – sequence: 5 givenname: Raul Yhossef surname: Tito fullname: Tito, Raul Yhossef organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Molecular Bacteriology, Leuven, Belgium, Center for Microbiology, VIB, Leuven, Belgium – sequence: 6 givenname: Mireia surname: Valles-Colomer fullname: Valles-Colomer, Mireia organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Molecular Bacteriology, Leuven, Belgium, Center for Microbiology, VIB, Leuven, Belgium, CIBIO-University of Trento, Povo, Trento, Italy – sequence: 7 givenname: Leen surname: Rymenans fullname: Rymenans, Leen organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Molecular Bacteriology, Leuven, Belgium, Center for Microbiology, VIB, Leuven, Belgium – sequence: 8 givenname: Daan orcidid: 0000-0003-4612-6891 surname: Jansen fullname: Jansen, Daan organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Viral Metagenomics, Leuven, Belgium – sequence: 9 givenname: Lore orcidid: 0000-0002-3870-4551 surname: Van Espen fullname: Van Espen, Lore organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Viral Metagenomics, Leuven, Belgium – sequence: 10 givenname: Maria Ioanna surname: Papadaki fullname: Papadaki, Maria Ioanna organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Viral Metagenomics, Leuven, Belgium – sequence: 11 givenname: Chenyan surname: Shi fullname: Shi, Chenyan organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Viral Metagenomics, Leuven, Belgium – sequence: 12 givenname: Claude Kwe orcidid: 0000-0002-5195-5478 surname: Yinda fullname: Yinda, Claude Kwe organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Viral Metagenomics, Leuven, Belgium, NIAID/NIH, Rocky Mountain Laboratories, Laboratory of Virology, Virus Ecology Unit, Hamilton, Montana, USA – sequence: 13 givenname: Mark surname: Zeller fullname: Zeller, Mark organization: Department of Immunology and Microbiology, Scripps Research, La Jolla, California, USA – sequence: 14 givenname: Karoline surname: Faust fullname: Faust, Karoline organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Molecular Bacteriology, Leuven, Belgium – sequence: 15 givenname: Marc surname: Van Ranst fullname: Van Ranst, Marc organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, Leuven, Belgium – sequence: 16 givenname: Jeroen surname: Raes fullname: Raes, Jeroen organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Molecular Bacteriology, Leuven, Belgium, Center for Microbiology, VIB, Leuven, Belgium – sequence: 17 givenname: Jelle orcidid: 0000-0003-1188-9733 surname: Matthijnssens fullname: Matthijnssens, Jelle organization: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Viral Metagenomics, Leuven, Belgium |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34903050$$D View this record in MEDLINE/PubMed |
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Keywords | microbiota infant primary succession enterotypes |
Language | English |
License | This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Jeroen Raes and Jelle Matthijnssens contributed equally. The authors declare no conflict of interest. |
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Snippet | After birth, microbial colonization of the infant intestinal tract is important for health later in life. However, this initial process is highly dynamic and... Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host conditions.... ABSTRACT Disturbances in the primary colonization of the infant gut can result in lifelong consequences and have been associated with a range of host... |
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SubjectTerms | Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Bacteriology Cohort Studies enterotypes Feces - microbiology Female Gastrointestinal Microbiome Gastrointestinal Tract - microbiology Humans Infant Infant, Newborn - growth & development Male microbiota primary succession Research Article |
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Title | Successional Stages in Infant Gut Microbiota Maturation |
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