Cargando…

Colonization and Succession within the Human Gut Microbiome by Archaea, Bacteria, and Microeukaryotes during the First Year of Life

Perturbations to the colonization process of the human gastrointestinal tract have been suggested to result in adverse health effects later in life. Although much research has been performed on bacterial colonization and succession, much less is known about the other two domains of life, archaea, an...

Descripción completa

Detalles Bibliográficos
Autores principales: Wampach, Linda, Heintz-Buschart, Anna, Hogan, Angela, Muller, Emilie E. L., Narayanasamy, Shaman, Laczny, Cedric C., Hugerth, Luisa W., Bindl, Lutz, Bottu, Jean, Andersson, Anders F., de Beaufort, Carine, Wilmes, Paul
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5411419/
https://www.ncbi.nlm.nih.gov/pubmed/28512451
http://dx.doi.org/10.3389/fmicb.2017.00738
_version_ 1783232827588870144
author Wampach, Linda
Heintz-Buschart, Anna
Hogan, Angela
Muller, Emilie E. L.
Narayanasamy, Shaman
Laczny, Cedric C.
Hugerth, Luisa W.
Bindl, Lutz
Bottu, Jean
Andersson, Anders F.
de Beaufort, Carine
Wilmes, Paul
author_facet Wampach, Linda
Heintz-Buschart, Anna
Hogan, Angela
Muller, Emilie E. L.
Narayanasamy, Shaman
Laczny, Cedric C.
Hugerth, Luisa W.
Bindl, Lutz
Bottu, Jean
Andersson, Anders F.
de Beaufort, Carine
Wilmes, Paul
author_sort Wampach, Linda
collection PubMed
description Perturbations to the colonization process of the human gastrointestinal tract have been suggested to result in adverse health effects later in life. Although much research has been performed on bacterial colonization and succession, much less is known about the other two domains of life, archaea, and eukaryotes. Here we describe colonization and succession by bacteria, archaea and microeukaryotes during the first year of life (samples collected around days 1, 3, 5, 28, 150, and 365) within the gastrointestinal tract of infants delivered either vaginally or by cesarean section and using a combination of quantitative real-time PCR as well as 16S and 18S rRNA gene amplicon sequencing. Sequences from organisms belonging to all three domains of life were detectable in all of the collected meconium samples. The microeukaryotic community composition fluctuated strongly over time and early diversification was delayed in infants receiving formula milk. Cesarean section-delivered (CSD) infants experienced a delay in colonization and succession, which was observed for all three domains of life. Shifts in prokaryotic succession in CSD infants compared to vaginally delivered (VD) infants were apparent as early as days 3 and 5, which were characterized by increased relative abundances of the genera Streptococcus and Staphylococcus, and a decrease in relative abundance for the genera Bifidobacterium and Bacteroides. Generally, a depletion in Bacteroidetes was detected as early as day 5 postpartum in CSD infants, causing a significantly increased Firmicutes/Bacteroidetes ratio between days 5 and 150 when compared to VD infants. Although the delivery mode appeared to have the strongest influence on differences between the infants, other factors such as a younger gestational age or maternal antibiotics intake likely contributed to the observed patterns as well. Our findings complement previous observations of a delay in colonization and succession of CSD infants, which affects not only bacteria but also archaea and microeukaryotes. This further highlights the need for resolving bacterial, archaeal, and microeukaryotic dynamics in future longitudinal studies of microbial colonization and succession within the neonatal gastrointestinal tract.
format Online
Article
Text
id pubmed-5411419
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-54114192017-05-16 Colonization and Succession within the Human Gut Microbiome by Archaea, Bacteria, and Microeukaryotes during the First Year of Life Wampach, Linda Heintz-Buschart, Anna Hogan, Angela Muller, Emilie E. L. Narayanasamy, Shaman Laczny, Cedric C. Hugerth, Luisa W. Bindl, Lutz Bottu, Jean Andersson, Anders F. de Beaufort, Carine Wilmes, Paul Front Microbiol Microbiology Perturbations to the colonization process of the human gastrointestinal tract have been suggested to result in adverse health effects later in life. Although much research has been performed on bacterial colonization and succession, much less is known about the other two domains of life, archaea, and eukaryotes. Here we describe colonization and succession by bacteria, archaea and microeukaryotes during the first year of life (samples collected around days 1, 3, 5, 28, 150, and 365) within the gastrointestinal tract of infants delivered either vaginally or by cesarean section and using a combination of quantitative real-time PCR as well as 16S and 18S rRNA gene amplicon sequencing. Sequences from organisms belonging to all three domains of life were detectable in all of the collected meconium samples. The microeukaryotic community composition fluctuated strongly over time and early diversification was delayed in infants receiving formula milk. Cesarean section-delivered (CSD) infants experienced a delay in colonization and succession, which was observed for all three domains of life. Shifts in prokaryotic succession in CSD infants compared to vaginally delivered (VD) infants were apparent as early as days 3 and 5, which were characterized by increased relative abundances of the genera Streptococcus and Staphylococcus, and a decrease in relative abundance for the genera Bifidobacterium and Bacteroides. Generally, a depletion in Bacteroidetes was detected as early as day 5 postpartum in CSD infants, causing a significantly increased Firmicutes/Bacteroidetes ratio between days 5 and 150 when compared to VD infants. Although the delivery mode appeared to have the strongest influence on differences between the infants, other factors such as a younger gestational age or maternal antibiotics intake likely contributed to the observed patterns as well. Our findings complement previous observations of a delay in colonization and succession of CSD infants, which affects not only bacteria but also archaea and microeukaryotes. This further highlights the need for resolving bacterial, archaeal, and microeukaryotic dynamics in future longitudinal studies of microbial colonization and succession within the neonatal gastrointestinal tract. Frontiers Media S.A. 2017-05-02 /pmc/articles/PMC5411419/ /pubmed/28512451 http://dx.doi.org/10.3389/fmicb.2017.00738 Text en Copyright © 2017 Wampach, Heintz-Buschart, Hogan, Muller, Narayanasamy, Laczny, Hugerth, Bindl, Bottu, Andersson, de Beaufort and Wilmes. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Wampach, Linda
Heintz-Buschart, Anna
Hogan, Angela
Muller, Emilie E. L.
Narayanasamy, Shaman
Laczny, Cedric C.
Hugerth, Luisa W.
Bindl, Lutz
Bottu, Jean
Andersson, Anders F.
de Beaufort, Carine
Wilmes, Paul
Colonization and Succession within the Human Gut Microbiome by Archaea, Bacteria, and Microeukaryotes during the First Year of Life
title Colonization and Succession within the Human Gut Microbiome by Archaea, Bacteria, and Microeukaryotes during the First Year of Life
title_full Colonization and Succession within the Human Gut Microbiome by Archaea, Bacteria, and Microeukaryotes during the First Year of Life
title_fullStr Colonization and Succession within the Human Gut Microbiome by Archaea, Bacteria, and Microeukaryotes during the First Year of Life
title_full_unstemmed Colonization and Succession within the Human Gut Microbiome by Archaea, Bacteria, and Microeukaryotes during the First Year of Life
title_short Colonization and Succession within the Human Gut Microbiome by Archaea, Bacteria, and Microeukaryotes during the First Year of Life
title_sort colonization and succession within the human gut microbiome by archaea, bacteria, and microeukaryotes during the first year of life
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5411419/
https://www.ncbi.nlm.nih.gov/pubmed/28512451
http://dx.doi.org/10.3389/fmicb.2017.00738
work_keys_str_mv AT wampachlinda colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT heintzbuschartanna colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT hoganangela colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT mulleremilieel colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT narayanasamyshaman colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT lacznycedricc colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT hugerthluisaw colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT bindllutz colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT bottujean colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT anderssonandersf colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT debeaufortcarine colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife
AT wilmespaul colonizationandsuccessionwithinthehumangutmicrobiomebyarchaeabacteriaandmicroeukaryotesduringthefirstyearoflife