Bacteroides abundance drives birth mode dependent infant gut microbiota developmental trajectories

Background and aimsBirth mode and other early life factors affect a newborn's microbial colonization with potential long-term health effects. Individual variations in early life gut microbiota development, especially their effects on the functional repertoire of microbiota, are still poorly cha...

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Main Authors: Dollwin Matharu, Alise J. Ponsero, Evgenia Dikareva, Katri Korpela, Kaija-Leena Kolho, Willem M. de Vos, Anne Salonen
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.953475/full
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author Dollwin Matharu
Alise J. Ponsero
Alise J. Ponsero
Evgenia Dikareva
Katri Korpela
Kaija-Leena Kolho
Kaija-Leena Kolho
Kaija-Leena Kolho
Willem M. de Vos
Willem M. de Vos
Anne Salonen
author_facet Dollwin Matharu
Alise J. Ponsero
Alise J. Ponsero
Evgenia Dikareva
Katri Korpela
Kaija-Leena Kolho
Kaija-Leena Kolho
Kaija-Leena Kolho
Willem M. de Vos
Willem M. de Vos
Anne Salonen
author_sort Dollwin Matharu
collection DOAJ
description Background and aimsBirth mode and other early life factors affect a newborn's microbial colonization with potential long-term health effects. Individual variations in early life gut microbiota development, especially their effects on the functional repertoire of microbiota, are still poorly characterized. This study aims to provide new insights into the gut microbiome developmental trajectories during the first year of life.MethodsOur study comprised 78 term infants sampled at 3 weeks, 3 months, 6 months, and 12 months (n = 280 total samples), and their mothers were sampled in late pregnancy (n = 50). Fecal DNA was subjected to shotgun metagenomic sequencing. Infant samples were studied for taxonomic and functional maturation, and maternal microbiota was used as a reference. Hierarchical clustering on taxonomic profiles was used to identify the main microbiota developmental trajectories in the infants, and their associations with perinatal and postnatal factors were assessed.ResultsIn line with previous studies, infant microbiota composition showed increased alpha diversity and decreased beta diversity by age, converging toward an adult-like profile. However, we did not observe an increase in functional alpha diversity, which was stable and comparable with the mother samples throughout all the sampling points. Using a de novo clustering approach, two main infant microbiota clusters driven by Bacteroidaceae and Clostridiaceae emerged at each time point. The clusters were associated with birth mode and their functions differed mainly in terms of biosynthetic and carbohydrate degradation pathways, some of which consistently differed between the clusters for all the time points. The longitudinal analysis indicated three main microbiota developmental trajectories, with the majority of the infants retaining their characteristic cluster until 1 year. As many as 40% of vaginally delivered infants were grouped with infants delivered by C-section due to their clear and persistent depletion in Bacteroides. Intrapartum antibiotics, any perinatal or postnatal factors, maternal microbiota composition, or other maternal factors did not explain the depletion in Bacteroides in the subset of vaginally born infants.ConclusionOur study provides an enhanced understanding of the compositional and functional early life gut microbiota trajectories, opening avenues for investigating elusive causes that influence non-typical microbiota development.
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spelling doaj.art-9763ca64fcab411883152843b7adcf2e2022-12-22T02:25:17ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-10-011310.3389/fmicb.2022.953475953475Bacteroides abundance drives birth mode dependent infant gut microbiota developmental trajectoriesDollwin Matharu0Alise J. Ponsero1Alise J. Ponsero2Evgenia Dikareva3Katri Korpela4Kaija-Leena Kolho5Kaija-Leena Kolho6Kaija-Leena Kolho7Willem M. de Vos8Willem M. de Vos9Anne Salonen10Human Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandDepartment of Biosystems Engineering and BIO5 Institute, University of Arizona, Tucson, AZ, United StatesHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandChildren's Hospital, Pediatric Research Center, University of Helsinki and HUS, Helsinki, FinlandFaculty of Medicine and Health Technology, University of Tampere, Tampere, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandLaboratory of Microbiology, Wageningen University, Wageningen, NetherlandsHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandBackground and aimsBirth mode and other early life factors affect a newborn's microbial colonization with potential long-term health effects. Individual variations in early life gut microbiota development, especially their effects on the functional repertoire of microbiota, are still poorly characterized. This study aims to provide new insights into the gut microbiome developmental trajectories during the first year of life.MethodsOur study comprised 78 term infants sampled at 3 weeks, 3 months, 6 months, and 12 months (n = 280 total samples), and their mothers were sampled in late pregnancy (n = 50). Fecal DNA was subjected to shotgun metagenomic sequencing. Infant samples were studied for taxonomic and functional maturation, and maternal microbiota was used as a reference. Hierarchical clustering on taxonomic profiles was used to identify the main microbiota developmental trajectories in the infants, and their associations with perinatal and postnatal factors were assessed.ResultsIn line with previous studies, infant microbiota composition showed increased alpha diversity and decreased beta diversity by age, converging toward an adult-like profile. However, we did not observe an increase in functional alpha diversity, which was stable and comparable with the mother samples throughout all the sampling points. Using a de novo clustering approach, two main infant microbiota clusters driven by Bacteroidaceae and Clostridiaceae emerged at each time point. The clusters were associated with birth mode and their functions differed mainly in terms of biosynthetic and carbohydrate degradation pathways, some of which consistently differed between the clusters for all the time points. The longitudinal analysis indicated three main microbiota developmental trajectories, with the majority of the infants retaining their characteristic cluster until 1 year. As many as 40% of vaginally delivered infants were grouped with infants delivered by C-section due to their clear and persistent depletion in Bacteroides. Intrapartum antibiotics, any perinatal or postnatal factors, maternal microbiota composition, or other maternal factors did not explain the depletion in Bacteroides in the subset of vaginally born infants.ConclusionOur study provides an enhanced understanding of the compositional and functional early life gut microbiota trajectories, opening avenues for investigating elusive causes that influence non-typical microbiota development.https://www.frontiersin.org/articles/10.3389/fmicb.2022.953475/fullBacteroidesshotgun metagenomicsinfant gut microbiotafunctional maturationhierarchical clusteringvaginal delivery
spellingShingle Dollwin Matharu
Alise J. Ponsero
Alise J. Ponsero
Evgenia Dikareva
Katri Korpela
Kaija-Leena Kolho
Kaija-Leena Kolho
Kaija-Leena Kolho
Willem M. de Vos
Willem M. de Vos
Anne Salonen
Bacteroides abundance drives birth mode dependent infant gut microbiota developmental trajectories
Frontiers in Microbiology
Bacteroides
shotgun metagenomics
infant gut microbiota
functional maturation
hierarchical clustering
vaginal delivery
title Bacteroides abundance drives birth mode dependent infant gut microbiota developmental trajectories
title_full Bacteroides abundance drives birth mode dependent infant gut microbiota developmental trajectories
title_fullStr Bacteroides abundance drives birth mode dependent infant gut microbiota developmental trajectories
title_full_unstemmed Bacteroides abundance drives birth mode dependent infant gut microbiota developmental trajectories
title_short Bacteroides abundance drives birth mode dependent infant gut microbiota developmental trajectories
title_sort bacteroides abundance drives birth mode dependent infant gut microbiota developmental trajectories
topic Bacteroides
shotgun metagenomics
infant gut microbiota
functional maturation
hierarchical clustering
vaginal delivery
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.953475/full
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