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


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2017-07-10

AUTHORS

Weili Xiong, Christopher T. Brown, Michael J. Morowitz, Jillian F. Banfield, Robert L. Hettich

ABSTRACT

BACKGROUND: 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). RESULTS: 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. CONCLUSIONS: 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. More... »

PAGES

72

References to SciGraph publications

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    37 schema:description BACKGROUND: 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). RESULTS: 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. CONCLUSIONS: 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.
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    45 Genome-resolved metaproteomic characterization
    46 Overall
    47 abundance
    48 abundant organisms
    49 acid
    50 acid production
    51 amino acids
    52 analysis
    53 approach
    54 birth
    55 carbohydrates
    56 characterization
    57 clusters
    58 colonization
    59 community
    60 complex microbial communities
    61 contribution
    62 development
    63 differences
    64 dissimilarity
    65 early colonization
    66 early life
    67 early-life microbiota development
    68 energy
    69 entire life span
    70 establishment
    71 fatty acid production
    72 fatty acids
    73 fecal samples
    74 function
    75 functional stability
    76 group
    77 gut
    78 gut communities
    79 gut microbiota
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    81 gut proteome profiles
    82 gut-specific metabolic module (GMM) analysis
    83 host physiology
    84 human gut microbiota
    85 human infant gut
    86 human proteins
    87 immune response
    88 increase
    89 individual fecal samples
    90 infancy
    91 infant gut
    92 infant gut microbiota development
    93 infant gut proteome profiles
    94 infants
    95 initial colonization
    96 inter-individual differences
    97 large-scale characterization
    98 levels
    99 life
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    101 major nutrient source
    102 maturation
    103 maximum percentage
    104 metabolic functions
    105 metabolic module (GMM) analysis
    106 metabolic shift
    107 metabolism
    108 metagenome-informed metaproteomic approach
    109 metagenomics
    110 metaproteomic approach
    111 metaproteomic characterization
    112 metaproteomics
    113 microbial EggNOG orthologous groups
    114 microbial colonization
    115 microbial communities
    116 microbial protein
    117 microbiota
    118 microbiota development
    119 microbiota-associated shifts
    120 module analysis
    121 mucosal maturation
    122 nucleotide metabolism
    123 nutrient source
    124 nutrient utilization
    125 organisms
    126 orthologous groups
    127 percentage
    128 physiology
    129 population structure
    130 preterm gut communities
    131 preterm human infants' gut
    132 preterm infant gut
    133 preterm infant gut microbiota development
    134 production
    135 profile
    136 protein
    137 protein abundance
    138 protein groups
    139 proteome
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    141 proteome profiles
    142 relative abundance
    143 relative protein abundance
    144 remarkable variation
    145 response
    146 samples
    147 shift
    148 short-chain fatty acid production
    149 short-chain fatty acids
    150 source
    151 span
    152 species-specific metabolic shifts
    153 species-specific proteome profiles
    154 species/
    155 stability
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    158 technology
    159 temporal shifts
    160 time
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