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Title: Genome-resolved metaproteomic characterization of preterm infant gut microbiota development reveals species-specific metabolic shifts and variabilities during early life

Journal Article · · Microbiome
ORCiD logo [1];  [2];  [3];  [2]; ORCiD logo [4]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  2. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
  3. Univ. of Pittsburgh, PA (United States). School of Medicine
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division

Establishment of the human gut microbiota begins at birth. This early-life microbiota development can impact host physiology during infancy and even across an entire life span. However, the functional stability and population structure of the gut microbiota during initial colonization remain poorly understood. Metaproteomics is an emerging technology for the large-scale characterization of metabolic functions in complex microbial communities (gut microbiota).We applied a metagenome-informed metaproteomic approach to study the temporal and inter-individual differences of metabolic functions during microbial colonization of preterm human infants' gut. By analyzing 30 individual fecal samples, we identified up to 12,568 protein groups for each of four infants, including both human and microbial proteins. With genome-resolved matched metagenomics, proteins were confidently identified at the species/strain level. The maximum percentage of the proteome detected for the abundant organisms was ~45%. A time-dependent increase in the relative abundance of microbial versus human proteins suggested increasing microbial colonization during the first few weeks of early life. We observed remarkable variations and temporal shifts in the relative protein abundances of each organism in these preterm gut communities. Given the dissimilarity of the communities, only 81 microbial EggNOG orthologous groups and 57 human proteins were observed across all samples. These conserved microbial proteins were involved in carbohydrate, energy, amino acid and nucleotide metabolism while conserved human proteins were related to immune response and mucosal maturation. We identified seven proteome clusters for the communities and showed infant gut proteome profiles were unstable across time and not individual-specific. Applying a gut-specific metabolic module (GMM) analysis, we found that gut communities varied primarily in the contribution of nutrient (carbohydrates, lipids, and amino acids) utilization and short-chain fatty acid production.Overall, this study reports species-specific proteome profiles and metabolic functions of human gut microbiota during early colonization. In particular, our work contributes to reveal microbiota-associated shifts and variations in the metabolism of three major nutrient sources and short-chain fatty acid during colonization of preterm infant gut.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE; National Institutes of Health (NIH)
Grant/Contract Number:
AC05-00OR22725; 1R01-GM-103600; AC02-05CH11231
OSTI ID:
1407990
Alternate ID(s):
OSTI ID: 1581162
Journal Information:
Microbiome, Vol. 5, Issue 1; ISSN 2049-2618
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 27 works
Citation information provided by
Web of Science

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Cited By (6)

Metaproteomic and Metabolomic Approaches for Characterizing the Gut Microbiome journal July 2019
Colonization of Cutibacterium avidum during infant gut microbiota establishment journal November 2018
A system biology perspective on environment–host–microbe interactions journal April 2018
Metaproteomics reveals persistent and phylum-redundant metabolic functional stability in adult human gut microbiomes of Crohn’s remission patients despite temporal variations in microbial taxa, genomes, and proteomes journal February 2019
Metaproteomic and 16S rRNA Gene Sequencing Analysis of the Infant Fecal Microbiome journal March 2019
Disseminating Metaproteomic Informatics Capabilities and Knowledge Using the Galaxy-P Framework journal January 2018