Abstract
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.
Highlights
The human microbiome contributes essential functionalities to human physiology and is thought to play a crucial role in governing human health and disease (Greenhalgh et al, 2016)
Sixty-five fecal samples were collected between September 2012 and April 2014 at the Centre Hospitalier de Luxembourg (CHL) from eight healthy vaginally delivered (VD) and seven healthy cesarean section delivery (CSD) infants at six time points
We found that generally lower amounts of DNA were extracted from stool of CSD infants compared to VD infants using the same extraction protocol, suggesting a delay in the acquisition of prokaryotic biomass in the gastrointestinal tract (GIT) of CSD infants
Summary
The human microbiome contributes essential functionalities to human physiology and is thought to play a crucial role in governing human health and disease (Greenhalgh et al, 2016). A growing body of evidence suggests that chronic diseases such as allergies (Abrahamsson et al, 2012, 2014), type 2 diabetes (Delzenne et al, 2015), obesity (Turnbaugh et al, 2006), and metabolic syndrome (Vrieze et al, 2012) are associated with a disequilibrium in the microbiome of the human gastrointestinal tract (GIT). Based on spatio-temporal studies in humans (Abrahamsson et al, 2014), it has been suggested that various disturbances in the initial microbiome colonization process as early as 1 month after birth may increase chronic disease susceptibilities over the course of human life (Arrieta et al, 2014; Cox et al, 2014; Houghteling and Walker, 2015). It has been previously observed that the delivery mode is the most important factor in determining the early colonization pattern(s) (Biasucci et al, 2008; Dominguez-Bello et al, 2010; Jakobsson et al, 2014; Rutayisire et al, 2016), other factors, such as diet (breast milk vs. formula milk; Le Huërou-Luron et al, 2010), gestational age (term delivery vs. preterm delivery; Barrett et al, 2013), or the maternal intake of antibiotics (Sekirov et al, 2008) have been observed to have effects on this process
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