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Phylogenetic and Metabolic Tracking of Gut Microbiota during Perinatal Development.

Del Chierico F, Vernocchi P, Petrucca A, Paci P, Fuentes S, Praticò G, Capuani G, Masotti A, Reddel S, Russo A, Vallone C, Salvatori G, Buffone E, Signore F, Rigon G, Dotta A, Miccheli A, de Vos WM, Dallapiccola B, Putignani L - PLoS ONE (2015)

Bottom Line: A cohort of 31 mother and neonate pairs, including 25 at-term caesarean (CS) and 6 vaginally (V) delivered neonates (DNs), were included in this study and 121 meconium/faecal samples were collected at days 1 through 30 following birth.A microbiota "core" of OTUs was identified that was independent of delivery mode and lactation stage, suggesting highly specialized communities that act as seminal colonizers of microbial networks.Correlations among OTUs, metabolites, and OTUs-metabolites revealed metabolic profiles associated with early microbial ecological dynamics, maturation of milk components, and host physiology.

View Article: PubMed Central - PubMed

Affiliation: Unit of Metagenomics, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.

ABSTRACT
The colonization and development of gut microbiota immediately after birth is highly variable and depends on several factors, such as delivery mode and modality of feeding during the first months of life. A cohort of 31 mother and neonate pairs, including 25 at-term caesarean (CS) and 6 vaginally (V) delivered neonates (DNs), were included in this study and 121 meconium/faecal samples were collected at days 1 through 30 following birth. Operational taxonomic units (OTUs) were assessed in 69 stool samples by phylogenetic microarray HITChip and inter- and intra-individual distributions were established by inter-OTUs correlation matrices and OTUs co-occurrence or co-exclusion networks. 1H-NMR metabolites were determined in 70 stool samples, PCA analysis was performed on 55 CS DNs samples, and metabolome/OTUs co-correlations were assessed in 45 CS samples, providing an integrated map of the early microbiota OTUs-metabolome. A microbiota "core" of OTUs was identified that was independent of delivery mode and lactation stage, suggesting highly specialized communities that act as seminal colonizers of microbial networks. Correlations among OTUs, metabolites, and OTUs-metabolites revealed metabolic profiles associated with early microbial ecological dynamics, maturation of milk components, and host physiology.

No MeSH data available.


Graphical representation of OTUs co-occurrence networks.Panel A shows the OTUs co-occurrence network for CS-delivered babies at 1–3 days following birth (see sheet B in S5 Table for details). Panel B shows OTUs co-occurrence network for CS-delivered babies at 7–30 days following birth (see sheet C in S5 Table for details). Panel C shows OTUs co-occurrence network for V-delivered babies at 1–3 days following birth (see sheet D in S5 Table for details). Red line indicates a positive correlation and a green line indicates a negative correlation. Pearson’s test was used to evaluate the correlation amongst OTUs (statistical significance was assessed with p<0.01).
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pone.0137347.g004: Graphical representation of OTUs co-occurrence networks.Panel A shows the OTUs co-occurrence network for CS-delivered babies at 1–3 days following birth (see sheet B in S5 Table for details). Panel B shows OTUs co-occurrence network for CS-delivered babies at 7–30 days following birth (see sheet C in S5 Table for details). Panel C shows OTUs co-occurrence network for V-delivered babies at 1–3 days following birth (see sheet D in S5 Table for details). Red line indicates a positive correlation and a green line indicates a negative correlation. Pearson’s test was used to evaluate the correlation amongst OTUs (statistical significance was assessed with p<0.01).

Mentions: In order to study the co-occurrence networks of the relative abundance of OTUs, microbial clusters were visualized for CS- and V-delivered babies at 1–3 days (Fig 4, Panels A, C) and CS-delivered babies at 7–30 days (Fig 4, Panel B). The central portion of each panel shows the gut microbiota “core”, represented by the network of OTUs with the highest clustering coefficient, a function related to the number of correlations that in most instances was positive. In Panel A, within the 130 OTUs framework, 124 positive and 53 negative correlations were found. In Panel B, 121 correlations were positive and 42 negative. In Panel C, 103 correlations were positive and 13 negative, confirming a reduced number of interactions in V-delivered compared to CS-delivered babies at days 1–3. One main cluster was present in CS-delivered babies at both 1–3 and 7–30 days, composed of 55 and 62 OTUs, respectively, while two clusters were identified in the V-delivered babies, composed of 33 (i.e., cluster A) and 13 OTUs (i.e., Bacteroidetes cluster B) (Sheet E in S5 Table). In order to assess the uniqueness of OTUs (single network-tailored structure) or, alternatively, commonness (network “core” structure), co-occurrence clusters were interpreted with reference to presence/absence in the CS 1–3, CS 7–30, and V 1–3 groups. The following gut microbiota network structures were identified: i) unique OTUs associated with the CS-delivered group at 1–3 days; ii) unique OTUs associated with the CS-delivered group at 7–30 days; iii) unique OTUs associated with the V-delivered group at 1–3 days; iv) OTUs shared by groups i and iii; v) OTUs shared by groups i and ii; vi) OTUs shared by all groups (S1 Fig; Sheet F in S5 Table). The “core” structure (i.e., structure vi) was composed of 30 stable microbiota (SM) OTUs belonging to: Actinobacteria (1), Bacteroidetes (4), Cyanobacteria (1), Firmicutes (19), Proteobacteria (4), and Spirochaetes (1) (Sheet F in S5 Table). The identification of a defined core, independently associated with the delivery mode and lactation stage, provides support for the Savage theory, which is based on the assembly of gut microbiota as a “niche-driven process” that results in the establishment of a SM, followed by variable microbiota (VM) [57].


Phylogenetic and Metabolic Tracking of Gut Microbiota during Perinatal Development.

Del Chierico F, Vernocchi P, Petrucca A, Paci P, Fuentes S, Praticò G, Capuani G, Masotti A, Reddel S, Russo A, Vallone C, Salvatori G, Buffone E, Signore F, Rigon G, Dotta A, Miccheli A, de Vos WM, Dallapiccola B, Putignani L - PLoS ONE (2015)

Graphical representation of OTUs co-occurrence networks.Panel A shows the OTUs co-occurrence network for CS-delivered babies at 1–3 days following birth (see sheet B in S5 Table for details). Panel B shows OTUs co-occurrence network for CS-delivered babies at 7–30 days following birth (see sheet C in S5 Table for details). Panel C shows OTUs co-occurrence network for V-delivered babies at 1–3 days following birth (see sheet D in S5 Table for details). Red line indicates a positive correlation and a green line indicates a negative correlation. Pearson’s test was used to evaluate the correlation amongst OTUs (statistical significance was assessed with p<0.01).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4557834&req=5

pone.0137347.g004: Graphical representation of OTUs co-occurrence networks.Panel A shows the OTUs co-occurrence network for CS-delivered babies at 1–3 days following birth (see sheet B in S5 Table for details). Panel B shows OTUs co-occurrence network for CS-delivered babies at 7–30 days following birth (see sheet C in S5 Table for details). Panel C shows OTUs co-occurrence network for V-delivered babies at 1–3 days following birth (see sheet D in S5 Table for details). Red line indicates a positive correlation and a green line indicates a negative correlation. Pearson’s test was used to evaluate the correlation amongst OTUs (statistical significance was assessed with p<0.01).
Mentions: In order to study the co-occurrence networks of the relative abundance of OTUs, microbial clusters were visualized for CS- and V-delivered babies at 1–3 days (Fig 4, Panels A, C) and CS-delivered babies at 7–30 days (Fig 4, Panel B). The central portion of each panel shows the gut microbiota “core”, represented by the network of OTUs with the highest clustering coefficient, a function related to the number of correlations that in most instances was positive. In Panel A, within the 130 OTUs framework, 124 positive and 53 negative correlations were found. In Panel B, 121 correlations were positive and 42 negative. In Panel C, 103 correlations were positive and 13 negative, confirming a reduced number of interactions in V-delivered compared to CS-delivered babies at days 1–3. One main cluster was present in CS-delivered babies at both 1–3 and 7–30 days, composed of 55 and 62 OTUs, respectively, while two clusters were identified in the V-delivered babies, composed of 33 (i.e., cluster A) and 13 OTUs (i.e., Bacteroidetes cluster B) (Sheet E in S5 Table). In order to assess the uniqueness of OTUs (single network-tailored structure) or, alternatively, commonness (network “core” structure), co-occurrence clusters were interpreted with reference to presence/absence in the CS 1–3, CS 7–30, and V 1–3 groups. The following gut microbiota network structures were identified: i) unique OTUs associated with the CS-delivered group at 1–3 days; ii) unique OTUs associated with the CS-delivered group at 7–30 days; iii) unique OTUs associated with the V-delivered group at 1–3 days; iv) OTUs shared by groups i and iii; v) OTUs shared by groups i and ii; vi) OTUs shared by all groups (S1 Fig; Sheet F in S5 Table). The “core” structure (i.e., structure vi) was composed of 30 stable microbiota (SM) OTUs belonging to: Actinobacteria (1), Bacteroidetes (4), Cyanobacteria (1), Firmicutes (19), Proteobacteria (4), and Spirochaetes (1) (Sheet F in S5 Table). The identification of a defined core, independently associated with the delivery mode and lactation stage, provides support for the Savage theory, which is based on the assembly of gut microbiota as a “niche-driven process” that results in the establishment of a SM, followed by variable microbiota (VM) [57].

Bottom Line: A cohort of 31 mother and neonate pairs, including 25 at-term caesarean (CS) and 6 vaginally (V) delivered neonates (DNs), were included in this study and 121 meconium/faecal samples were collected at days 1 through 30 following birth.A microbiota "core" of OTUs was identified that was independent of delivery mode and lactation stage, suggesting highly specialized communities that act as seminal colonizers of microbial networks.Correlations among OTUs, metabolites, and OTUs-metabolites revealed metabolic profiles associated with early microbial ecological dynamics, maturation of milk components, and host physiology.

View Article: PubMed Central - PubMed

Affiliation: Unit of Metagenomics, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.

ABSTRACT
The colonization and development of gut microbiota immediately after birth is highly variable and depends on several factors, such as delivery mode and modality of feeding during the first months of life. A cohort of 31 mother and neonate pairs, including 25 at-term caesarean (CS) and 6 vaginally (V) delivered neonates (DNs), were included in this study and 121 meconium/faecal samples were collected at days 1 through 30 following birth. Operational taxonomic units (OTUs) were assessed in 69 stool samples by phylogenetic microarray HITChip and inter- and intra-individual distributions were established by inter-OTUs correlation matrices and OTUs co-occurrence or co-exclusion networks. 1H-NMR metabolites were determined in 70 stool samples, PCA analysis was performed on 55 CS DNs samples, and metabolome/OTUs co-correlations were assessed in 45 CS samples, providing an integrated map of the early microbiota OTUs-metabolome. A microbiota "core" of OTUs was identified that was independent of delivery mode and lactation stage, suggesting highly specialized communities that act as seminal colonizers of microbial networks. Correlations among OTUs, metabolites, and OTUs-metabolites revealed metabolic profiles associated with early microbial ecological dynamics, maturation of milk components, and host physiology.

No MeSH data available.