Dataset Information

Phylogenetic and Metabolic Tracking of Gut Microbiota during Perinatal Development.

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.

SUBMITTER: Del Chierico F

PROVIDER: S-EPMC4557834 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Phylogenetic and Metabolic Tracking of Gut Microbiota during Perinatal Development.

Del Chierico Federica F Vernocchi Pamela P Petrucca Andrea A Paci Paola P Fuentes Susana S Praticò Giulia G Capuani Giorgio G Masotti Andrea A Reddel Sofia S Russo Alessandra A Vallone Cristina C Salvatori Guglielmo G Buffone Elsa E Signore Fabrizio F Rigon Giuliano G Dotta Andrea A Miccheli Alfredo A de Vos Willem M WM Dallapiccola Bruno B Putignani Lorenza L

PloS one 20150902 9

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 stoo ...[more]

PMID: 26332837

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Project description:In humans, the metabolic and immune changes occurring during perinatal period also describe metabolic syndrome. Gut microbiota can cause symptoms of metabolic syndrome in pregnant women. Increased gut permeability is also involved in metabolic disorders in non-pregnant hosts. However, longitudinal studies investigating the changes in metabolic characteristics, gut microbiota, and gut permeability of sows throughout pregnancy and lactation are lacking. The correlation between gut microbiota and metabolic status of sows is also poorly known. The present study was conducted to investigate the temporal variations in sow metabolic characteristics, gut microbiota, gut permeability, and gut inflammation at days 30 (G30) and 109 (G109) of gestation and days 3 (L3) and 14 (L14) of lactation. Results showed that insulin sensitivity was decreased in L3. Circulating concentrations of pro-inflammatory cytokine IL-6 increased in G109 and L3. 16S rRNA gene sequencing of the V3-V4 region showed that gut microbiota changed dramatically across different reproductive stages. The bacterial abundance and alpha diversity in L3 were the lowest. The phyla Proteobacteria and Fusobacteria exhibited the highest relative abundance in L3. Among the genera, Bacteroides, Escherichia_Shigella, and Fusobacterium were highest, but Oscillospira the lowest, in relative abundance in L3. The fecal levels of acetate and total short-chain fatty acids were increased in G109, but fecal butyrate concentrations were markedly decreased in L3. The plasma zonulin concentrations, a biomarker for gut permeability, were increased in G109 and L3. The plasma endotoxin concentrations were increased in L3. Furthermore, levels of fecal lipocalin-2 and pro-inflammatory cytokines IL-6 and TNF-α were increased in G109 and L3. In contrast, fecal levels of anti-inflammatory cytokine IL-10 were significantly decreased in G109 and L3. Additionally, the increased relative abundances of Fusobacterium in L3 were positively correlated with plasma zonulin and fecal endotoxin but negatively correlated with fecal IL-10. These findings indicate that the mother sow exhibits a metabolic syndrome and dramatical changes in gut microbiota during perinatal period, especially in early lactation. Besides, increased gut permeability and plasma endotoxin concentrations caused by negative microbial changes would possibly be the potential mechanisms under which sow's metabolic disorders and inflammatory status were exacerbated during early lactation.

Project description:In recent decades, increasing evidence has strongly suggested that gut microbiota play an important role in many intestinal diseases including inflammatory bowel disease (IBD) and colorectal cancer (CRC). The composition of gut microbiota is thought to be largely shaped by interspecies competition for available resources and also by cooperative interactions. However, to what extent the changes could be attributed to external factors such as diet of choice and internal factors including mutual relationships among gut microbiota, respectively, are yet to be elucidated. Due to the advances of high-throughput sequencing technologies, flood of (meta)-genome sequence information and high-throughput biological data are available for gut microbiota and their association with intestinal diseases, making it easier to gain understanding of microbial physiology at the systems level. In addition, the newly developed genome-scale metabolic models that cover significant proportion of known gut microbes enable researchers to analyze and simulate the system-level metabolic response in response to different stimuli in the gut, providing deeper biological insights. Using metabolic interaction network based on pair-wise metabolic dependencies, we found the same interaction pattern in two IBD datasets and one CRC datasets. We report here for the first time that the growth of significantly enriched bacteria in IBD and CRC patients could be boosted by other bacteria including other significantly increased ones. Conversely, the growth of probiotics could be strongly inhibited from other species, including other probiotics. Therefore, it is very important to take the mutual interaction of probiotics into consideration when developing probiotics or "microbial based therapies." Together, our metabolic interaction network analysis can predict majority of the changes in terms of the changed directions in the gut microbiota during enteropathogenesis. Our results thus revealed unappreciated interaction patterns between species could underlie alterations in gut microbiota during enteropathogenesis, and between probiotics and other microbes. Our methods provided a new framework for studying interactions in gut microbiome and their roles in health and disease.

Project description:BackgroundObesity induced by a high-caloric diet has previously been associated with changes in the gut microbiota in mice and in humans. In this study, pigs were cloned to minimize genetic and biological variation among the animals with the aim of developing a controlled metabolomic model suitable for a diet-intervention study. Cloning of pigs may be an attractive way to reduce genetic influences when investigating the effect of diet and obesity on different physiological sites. The aim of this study was to assess and compare the changes in the composition of the gut microbiota of cloned vs. non-cloned pigs during development of obesity by a high-fat/high-caloric diet. Furthermore, we investigated the association between diet-induced obesity and the relative abundance of the phyla Firmicutes and Bacteroidetes in the fecal-microbiota. The fecal microbiota from obese cloned (n = 5) and non-cloned control pigs (n= 6) was investigated biweekly over a period of 136 days, by terminal restriction fragment length polymorphism (T-RFLP) and quantitative real time PCR (qPCR).ResultsA positive correlation was observed between body-weight at endpoint and percent body-fat in cloned (r=0.9, P<0.0001) and in non-cloned control pigs (r=0.9, P<0.0001). Shannon Weaver and principal component analysis (PCA) of the terminal restriction fragments (T-RFs) revealed no differences in the bacterial composition or variability of the fecal microbiota between the cloned pigs or between cloned and non-cloned control pigs. Body-weight correlated positively with the relative abundance of Firmicutes in both cloned (r=0.37; P<0.02) and non cloned-control pigs (r=0.45; P<0.006), and negatively with the abundance of Bacteroidetes in cloned pigs (r=-0.33, P<0.04), but not in the non-cloned control pigs.ConclusionThe cloned pigs did not have reduced inter-individual variation as compared to non-cloned pigs in regard to their gut microbiota in neither the obese nor the lean state. Diet-induced obesity was associated with an increase in the relative abundance of Firmicutes over time. Our results suggest that cloned pigs are not a more suitable animal model for gut microbiota-obesity related studies than non-cloned pigs. This study is the first to evaluate if cloned pigs provide a better animal model than conventional pigs in diet-intervention, obesity and gut microbiota research.

Project description:BackgroundThe gut microbiota potentially plays an important role in the immunologic education of the host during early infancy.ObjectiveWe sought to determine how the infant gut microbiota evolve during infancy, particularly in relation to hygiene-related environmental factors, atopic disorders, and a randomized introduction of allergenic solids.MethodsA total of 1303 exclusively breast-fed infants were enrolled in a dietary randomized controlled trial (Enquiring About Tolerance study) from 3 months of age. In this nested longitudinal study, fecal samples were collected at baseline, with additional sampling of selected cases and controls at 6 and 12 months to study the evolution of their gut microbiota, using 16S ribosomal RNA gene-targeted amplicon sequencing.ResultsIn the 288 baseline samples from exclusively breast-fed infant at 3 months, the gut microbiota was highly heterogeneous, forming 3 distinct clusters: Bifidobacterium-rich, Bacteroides-rich, and Escherichia/Shigella-rich. Mode of delivery was the major discriminating factor. Increased Clostridium sensu stricto relative abundance at 3 months was associated with presence of atopic dermatitis on examination at age 3 and 12 months. From the selected cases and controls with longitudinal samples (n = 70), transition to Bacteroides-rich communities and influx of adult-specific microbes were observed during the first year of life. The introduction of allergenic solids promoted a significant increase in Shannon diversity and representation of specific microbes, such as genera belonging to Prevotellaceae and Proteobacteria (eg, Escherichia/Shigella), as compared with infants recommended to exclusively breast-feed.ConclusionsSpecific gut microbiota characteristics of samples from 3-month-old breast-fed infants were associated with cesarean birth, and greater Clostridium sensu stricto abundance was associated with atopic dermatitis. The randomized introduction of allergenic solids from age 3 months alongside breast-feeding was associated with differential dynamics of maturation of the gut microbial communities.

Dataset Information

Phylogenetic and Metabolic Tracking of Gut Microbiota during Perinatal Development.

Publications

Phylogenetic and Metabolic Tracking of Gut Microbiota during Perinatal Development.

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