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. 2013 Jan;23(1):111-20.
doi: 10.1101/gr.142315.112. Epub 2012 Aug 30.

Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization

Itai Sharon  1 , Michael J Morowitz, Brian C Thomas, Elizabeth K Costello, David A Relman, Jillian F Banfield
Affiliations

Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization

Itai Sharon et al. Genome Res. 2013 Jan.

Abstract

The gastrointestinal microbiome undergoes shifts in species and strain abundances, yet dynamics involving closely related microorganisms remain largely unknown because most methods cannot resolve them. We developed new metagenomic methods and utilized them to track species and strain level variations in microbial communities in 11 fecal samples collected from a premature infant during the first month of life. Ninety six percent of the sequencing reads were assembled into scaffolds of >500 bp in length that could be assigned to organisms at the strain level. Six essentially complete (∼99%) and two near-complete genomes were assembled for bacteria that comprised as little as 1% of the community, as well as nine partial genomes of bacteria representing as little as 0.05%. In addition, three viral genomes were assembled and assigned to their hosts. The relative abundance of three Staphylococcus epidermidis strains, as well as three phages that infect them, changed dramatically over time. Genes possibly related to these shifts include those for resistance to antibiotics, heavy metals, and phage. At the species level, we observed the decline of an early-colonizing Propionibacterium acnes strain similar to SK137 and the proliferation of novel Propionibacterium and Peptoniphilus species late in colonization. The Propionibacterium species differed in their ability to metabolize carbon compounds such as inositol and sialic acid, indicating that shifts in species composition likely impact the metabolic potential of the community. These results highlight the benefit of reconstructing complete genomes from metagenomic data and demonstrate methods for achieving this goal.

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Figures

Figure 1.
Figure 1.
Time series-based ESOM binning of the whole data set (left) and Staphylococcus scaffolds (right). (Left) An ESOM in which each point represents a 500- to 6000-bp segment. Data points are colored based on their scaffold's best hit from all published genomes in the NCBI nucleotide database (white data points have no significant hit). Note that the map is periodic. Clusters are: 1. Candida albicans; 2. Finegoldia magna; 3. Staphylococcus hominis; 4. Staphylococcus lugdunensis; 5. Leuconostoc citreum; 6. Peptoniphilus Carrol (novel species); 7. Staphylococcus aureus; 8. Propionibacterium Carrol (novel species); 8.1 Propionibacterium acnes; 9. Streptococcus; 10. Staphylococcus epidermidis, regions on the genome that are common to all strains; 10.1 strain 1 and some low abundance scaffolds that probably belong to rare S. epidermidis strains; 10.3. regions unique to S. epidermidis strain 3; 10.4. regions unique to S. epidermidis strain 4; 11. Enterococcus faecalis; and 12. Anaerococcus. (Right) An ESOM of the Staphylococcus genomes (numbers are the same as in the left panel), their plasmids (extension “P”) and infecting phage (A: phage 13; B: phage 14; and C: phage 46). For S. epidermidis strain 1, dark red represents segments unique to the strain, while light red represents regions common to both strain 1 and strain 3 (likewise dark/light green for strain 3).
Figure 2.
Figure 2.
Relative abundance in the community of abundant (left) and rare (right) species. Abundance was computed based on read mapping to unique regions on the assembled genomes.
Figure 3.
Figure 3.
Abundance patterns of the Staphylococcus epidermidis strains (thick lines) and their infecting phage (thin dashed lines). All three phages exist primarily as prophages but also were identified as free-existing phages. Insertion positions are in regions that are shared by both abundant strains (and probably also by strain 4), but abundance patterns suggest that phage 13 and 14 infect strain 1, while phage 46 infects strain 3.
Figure 4.
Figure 4.
Abundance patterns of Propionibacterium-related genomes and their alignment against P. acnes SK137. (Left) Abundance of Propi. Carrol (red) and P. acnes (blue) as well as one Propionibacterium phage (green). The phage could not be linked to any of the species, either through integration site or through its abundance pattern. (Right) Alignment of both Propi. Carrol and P. acnes species to the genome of the skin P. acnes SK137.
Figure 5.
Figure 5.
Comparison of selected functionalities that differentiate Propi. Carrol and P. acnes SK137.
Figure 6.
Figure 6.
Analysis pipeline for metagenomic data employed in this study. Refer to the Methods section and the supporting online material for more details.
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