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Longitudinal analysis reveals transition barriers between dominant ecological states in the gut microbiome.

ABSTRACT: The Pioneer 100 Wellness Project involved quantitatively profiling 108 participants' molecular physiology over time, including genomes, gut microbiomes, blood metabolomes, blood proteomes, clinical chemistries, and data from wearable devices. Here, we present a longitudinal analysis focused specifically around the Pioneer 100 gut microbiomes. We distinguished a subpopulation of individuals with reduced gut diversity, elevated relative abundance of the genus Prevotella, and reduced levels of the genus Bacteroides We found that the relative abundances of Bacteroides and Prevotella were significantly correlated with certain serum metabolites, including omega-6 fatty acids. Primary dimensions in distance-based redundancy analysis of clinical chemistries explained 18.5% of the variance in bacterial community composition, and revealed a Bacteroides/Prevotella dichotomy aligned with inflammation and dietary markers. Finally, longitudinal analysis of gut microbiome dynamics within individuals showed that direct transitions between Bacteroides-dominated and Prevotella-dominated communities were rare, suggesting the presence of a barrier between these states. One implication is that interventions seeking to transition between Bacteroides- and Prevotella-dominated communities will need to identify permissible paths through ecological state-space that circumvent this apparent barrier.

SUBMITTER: Levy R

PROVIDER: S-EPMC7306764 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Longitudinal analysis reveals transition barriers between dominant ecological states in the gut microbiome.

Levy Roie R Magis Andrew T AT Earls John C JC Manor Ohad O Wilmanski Tomasz T Lovejoy Jennifer J Gibbons Sean M SM Omenn Gilbert S GS Hood Leroy L Price Nathan D ND

Proceedings of the National Academy of Sciences of the United States of America 20200529 24

The Pioneer 100 Wellness Project involved quantitatively profiling 108 participants' molecular physiology over time, including genomes, gut microbiomes, blood metabolomes, blood proteomes, clinical chemistries, and data from wearable devices. Here, we present a longitudinal analysis focused specifically around the Pioneer 100 gut microbiomes. We distinguished a subpopulation of individuals with reduced gut diversity, elevated relative abundance of the genus <i>Prevotella</i>, and reduced levels ...[more]

PMID: 32471946

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Project description:BackgroundThe infant microbiome contributes to health status across the lifespan, but environmental factors affecting microbial communities are poorly understood, particularly when toxic and essential elements interact.ObjectiveWe aimed to identify the associations between a spectrum of other early-postnatal nutrient or toxic elemental exposures measured and the infant gut microbiome.MethodsOur analysis included 179 six-week-old infants from the New Hampshire Birth Cohort Study. Eleven elements were measured in infant toenail clippings. The gut microbiome was assessed using 16S rRNA V4-V5 hypervariable region targeted sequencing. Multivariable zero-inflated logistic normal regression (MZILN) was used to model the association between element concentrations and taxon relative abundance. To explore interactive and nonlinear associations between the exposures and specific taxa we employed Bayesian Kernel Machine Regression (BKMR). Effect modification by delivery mode, feeding mode, peripartum antibiotic exposure, and infant sex was assessed with stratified models.ResultsWe found a negative association between arsenic and microbial diversity in the full population that was accentuated among infants exposed to peripartum antibiotics. Arsenic, cadmium, copper, iron, lead, manganese, nickel, selenium, tin, and zinc were each associated with differences in at least one taxon in the full study population, with most of the related taxa belonging to the Bacteroides and Lactobacillales. In stratified analyses, mercury, in addition to the other elements, was associated with specific taxa. Bifidobacterium, which associated negatively with zinc in MZILN and BKMR models, had a quadratic association with arsenic concentrations. These associations varied with the concentration of the other element.ConclusionsEarly postnatal toxic and nutrient elemental exposures are associated with differences in the infant microbiome. Further research is needed to clarify the whether these alterations are a biomarker of exposure or if they have implications for child and lifelong health.

Project description:BackgroundThe infant gut microbiome undergoes rapid changes in the first year of life, supporting normal development and long-term health. Although diet shapes this process, the role of fibers in complementary foods on gut microbiome maturation is poorly understood.ObjectivesWe explored how the transition from human milk to fibers in complementary foods shapes the taxonomic and functional maturation of the gut microbiome within the first year of life.MethodsWe assessed the longitudinal and cross-sectional development of infant gut microbiomes (N = 68 infants) and metabolomes (N = 33 infants) using linear mixed models to uncover their associations to dietary fibers and their food sources. Fiber intakes were assessed with 3-d food records (months 3, 6, 9, and 12) relying on CODEX-compliant fiber fraction values, and questionnaires tracked the overall complementary food introduction. Bacterial species were identified and quantified via MetaPhlAn2 from metagenomic data, and metabolomic profiles were obtained using 4 LC-MS methods.ResultsWe identified 176 complementary food fiber-bacterial species associations. First plant-based fibers associated with microbiota compositions similar to breastfeeding, and further associated with aromatic amino acid-derived metabolites, including 5-hydroxyindoleacetic acid (total dietary fiber - complementary foods (g) - β = 3.50, CI: 2.48, 4.52, P = 6.53 × 10-5). Distinct fibers from different food categories showed unique associations with specific bacterial taxa. Key species, such as Faecalibacterium prausnitznii, associated with oat fibers (g/MJ, β = 2.18, confidence interval: 1.36, 2.84, P = 6.12 × 10-6), reflective of maturing microbial communities. Fiber intake during weaning associated with shifts in metabolite profiles, including immunomodulatory metabolites, with fiber effects observed in a source- and timing-dependent manner, implicated in gradual microbiome diversification.ConclusionsIntroducing complementary dietary fibers during the weaning period supports gut microbiome diversification and stabilization. Even minor dietary variations shows significant associations with microbial taxa and functions from the onset of weaning, highlighting the importance of infant dietary recommendations that support the gut microbiome maturation during early life. This trial was registered at clinicaltrials.gov as registration number NCT01735123.

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Longitudinal analysis reveals transition barriers between dominant ecological states in the gut microbiome.

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Longitudinal analysis reveals transition barriers between dominant ecological states in the gut microbiome.

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