Genome resolved analysis of a premature infant gut microbial community reveals a Varibaculum cambriense genome and a shift towards fermentation-based ... View Full Text


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Article Info

DATE

2013-12-17

AUTHORS

Christopher T Brown, Itai Sharon, Brian C Thomas, Cindy J Castelle, Michael J Morowitz, Jillian F Banfield

ABSTRACT

BACKGROUND: The premature infant gut has low individual but high inter-individual microbial diversity compared with adults. Based on prior 16S rRNA gene surveys, many species from this environment are expected to be similar to those previously detected in the human microbiota. However, the level of genomic novelty and metabolic variation of strains found in the infant gut remains relatively unexplored. RESULTS: To study the stability and function of early microbial colonizers of the premature infant gut, nine stool samples were taken during the third week of life of a premature male infant delivered via Caesarean section. Metagenomic sequences were assembled and binned into near-complete and partial genomes, enabling strain-level genomic analysis of the microbial community.We reconstructed eleven near-complete and six partial bacterial genomes representative of the key members of the microbial community. Twelve of these genomes share >90% putative ortholog amino acid identity with reference genomes. Manual curation of the assembly of one particularly novel genome resulted in the first essentially complete genome sequence (in three pieces, the order of which could not be determined due to a repeat) for Varibaculum cambriense (strain Dora), a medically relevant species that has been implicated in abscess formation.During the period studied, the microbial community undergoes a compositional shift, in which obligate anaerobes (fermenters) overtake Escherichia coli as the most abundant species. Other species remain stable, probably due to their ability to either respire anaerobically or grow by fermentation, and their capacity to tolerate fluctuating levels of oxygen. Metabolic predictions for V. cambriense suggest that, like other members of the microbial community, this organism is able to process various sugar substrates and make use of multiple different electron acceptors during anaerobic respiration. Genome comparisons within the family Actinomycetaceae reveal important differences related to respiratory metabolism and motility. CONCLUSIONS: Genome-based analysis provided direct insight into strain-specific potential for anaerobic respiration and yielded the first genome for the genus Varibaculum. Importantly, comparison of these de novo assembled genomes with closely related isolate genomes supported the accuracy of the metagenomic methodology. Over a one-week period, the early gut microbial community transitioned to a community with a higher representation of obligate anaerobes, emphasizing both taxonomic and metabolic instability during colonization. More... »

PAGES

30-30

References to SciGraph publications

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    30 schema:description BACKGROUND: The premature infant gut has low individual but high inter-individual microbial diversity compared with adults. Based on prior 16S rRNA gene surveys, many species from this environment are expected to be similar to those previously detected in the human microbiota. However, the level of genomic novelty and metabolic variation of strains found in the infant gut remains relatively unexplored. RESULTS: To study the stability and function of early microbial colonizers of the premature infant gut, nine stool samples were taken during the third week of life of a premature male infant delivered via Caesarean section. Metagenomic sequences were assembled and binned into near-complete and partial genomes, enabling strain-level genomic analysis of the microbial community.We reconstructed eleven near-complete and six partial bacterial genomes representative of the key members of the microbial community. Twelve of these genomes share >90% putative ortholog amino acid identity with reference genomes. Manual curation of the assembly of one particularly novel genome resulted in the first essentially complete genome sequence (in three pieces, the order of which could not be determined due to a repeat) for Varibaculum cambriense (strain Dora), a medically relevant species that has been implicated in abscess formation.During the period studied, the microbial community undergoes a compositional shift, in which obligate anaerobes (fermenters) overtake Escherichia coli as the most abundant species. Other species remain stable, probably due to their ability to either respire anaerobically or grow by fermentation, and their capacity to tolerate fluctuating levels of oxygen. Metabolic predictions for V. cambriense suggest that, like other members of the microbial community, this organism is able to process various sugar substrates and make use of multiple different electron acceptors during anaerobic respiration. Genome comparisons within the family Actinomycetaceae reveal important differences related to respiratory metabolism and motility. CONCLUSIONS: Genome-based analysis provided direct insight into strain-specific potential for anaerobic respiration and yielded the first genome for the genus Varibaculum. Importantly, comparison of these de novo assembled genomes with closely related isolate genomes supported the accuracy of the metagenomic methodology. Over a one-week period, the early gut microbial community transitioned to a community with a higher representation of obligate anaerobes, emphasizing both taxonomic and metabolic instability during colonization.
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    37 schema:keywords Actinomycetaceae
    38 Escherichia coli
    39 Varibaculum
    40 Varibaculum cambriense
    41 Varibaculum cambriense genome
    42 ability
    43 abscess formation
    44 abundant species
    45 acceptor
    46 accuracy
    47 acid identity
    48 adults
    49 amino acid identity
    50 anaerobes
    51 anaerobes (fermenters) overtake Escherichia coli
    52 anaerobic respiration
    53 analysis
    54 assembly
    55 bacterial genomes representative
    56 caesarean section
    57 cambriense
    58 cambriense genome
    59 capacity
    60 coli
    61 colonization
    62 colonizers
    63 community
    64 comparison
    65 complete genome sequence
    66 compositional shifts
    67 curation
    68 de novo
    69 differences
    70 different electron acceptors
    71 direct insight
    72 diversity
    73 early gut microbial community
    74 early microbial colonizers
    75 electron acceptor
    76 environment
    77 family Actinomycetaceae
    78 fermentation
    79 fermentation-based metabolism
    80 first genome
    81 formation
    82 function
    83 gene surveys
    84 genome
    85 genome comparison
    86 genome sequence
    87 genomes representative
    88 genomic analysis
    89 genomic novelty
    90 genus Varibaculum
    91 gut
    92 gut microbial community
    93 high inter-individual microbial diversity
    94 high representation
    95 human microbiota
    96 identity
    97 important differences
    98 infant gut
    99 infant gut microbial community
    100 infants
    101 insights
    102 instability
    103 inter-individual microbial diversity
    104 isolate genomes
    105 key members
    106 levels
    107 levels of oxygen
    108 life
    109 male infant
    110 manual curation
    111 members
    112 metabolic instability
    113 metabolic predictions
    114 metabolic variations
    115 metabolism
    116 metagenomic methodologies
    117 metagenomic sequences
    118 methodology
    119 microbial colonizers
    120 microbial communities
    121 microbial diversity
    122 microbiota
    123 motility
    124 multiple different electron acceptors
    125 novel genomes
    126 novelty
    127 novo
    128 obligate anaerobes
    129 obligate anaerobes (fermenters) overtake Escherichia coli
    130 one-week period
    131 organisms
    132 ortholog amino acid identity
    133 overtake Escherichia coli
    134 oxygen
    135 partial bacterial genomes representative
    136 partial genomes
    137 period
    138 potential
    139 prediction
    140 premature infant gut
    141 premature infant gut microbial community
    142 premature male infant
    143 putative ortholog amino acid identity
    144 rRNA gene surveys
    145 reference genome
    146 relevant species
    147 representation
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    149 respiration
    150 respiratory metabolism
    151 samples
    152 sections
    153 sequence
    154 shift
    155 species
    156 stability
    157 stool samples
    158 strain-level genomic analysis
    159 strain-specific potential
    160 strains
    161 substrate
    162 sugar substrates
    163 survey
    164 third week
    165 use
    166 variation
    167 weeks
    168 schema:name Genome resolved analysis of a premature infant gut microbial community reveals a Varibaculum cambriense genome and a shift towards fermentation-based metabolism during the third week of life
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