Phage-bacteria interaction network in human oral microbiome

Summary Although increasing knowledge suggests that bacteriophages play important roles in regulating microbial ecosystems, phage–bacteria interaction in human oral cavities remains less understood. Here we performed a metagenomic analysis to explore the composition and variation of oral dsDNA phage...

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Published inEnvironmental microbiology Vol. 18; no. 7; pp. 2143 - 2158
Main Authors Wang, Jinfeng, Gao, Yuan, Zhao, Fangqing
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.07.2016
Wiley Subscription Services, Inc
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Summary:Summary Although increasing knowledge suggests that bacteriophages play important roles in regulating microbial ecosystems, phage–bacteria interaction in human oral cavities remains less understood. Here we performed a metagenomic analysis to explore the composition and variation of oral dsDNA phage populations and potential phage–bacteria interaction. A total of 1,711 contigs assembled with more than 100 Gb shotgun sequencing data were annotated to 104 phages based on their best BLAST matches against the NR database. Bray–Curtis dissimilarities demonstrated that both phage and bacterial composition are highly diverse between periodontally healthy samples but show a trend towards homogenization in diseased gingivae samples. Significantly, according to the CRISPR arrays that record infection relationship between bacteria and phage, we found certain oral phages were able to invade other bacteria besides their putative bacterial hosts. These cross‐infective phages were positively correlated with commensal bacteria while were negatively correlated with major periodontal pathogens, suggesting possible connection between these phages and microbial community structure in oral cavities. By characterizing phage–bacteria interaction as networks rather than exclusively pairwise predator–prey relationships, our study provides the first insight into the participation of cross‐infective phages in forming human oral microbiota.
Bibliography:Fig. S1. Numbers of ORFs in each putative phage contig. A contig was classified as a putative phage if all annotated ORFs in this contig were assigned to the phage or phage ORFs in this contig were more than annotated ORFs of any other phages. The number of phage ORFs in each contig is shown on x-axis and bacterial ORFs on y-axis. Each blue circle shows a putative phage contig. Circular area represents the number of unclassified ORFs within a contig. Fig. S2. Eight phage contigs presented nearly complete genomes. Colourized pentagons represent complete genes with known or unknown functions, and shaded pentagons represent partial genes. Peak charts show the length (x-axis) and coverage (y-axis) of contigs. The best-hit and sequence identity to reference phage genome (BLASTP) are given below each contig. Fig. S3. Phylogenetic analysis based on head (A) and tail proteins (B). Predicted gene sequences of head (blue nodes) and tail proteins (red nodes) were extracted from our contigs, translated to amino acids and built phylogenetic trees with homologous sequences of the NCBI database respectively. The numbers on the branching represent bootstrap values. Fig. S4. Fragments of a phage species connected with another bacterial species rather than its putative bacterial host. (A) A contig of our assemblies. (B and C) Contigs from the HMP. Pentagons with different color represent putative phage or bacterial genes. GenBank access number for each gene is given at the middle of each pentagon. Sequence identity (BLASTP) and the start and end position of each gene are shown above and below each pentagon respectively. Fig. S5. Percentages of phage families in saliva of periodontal health (PHS), dental plaque of periodontal health (PHP) and disease (PDP). (A) Composition of phage families measured in our study. (B) Composition of phage families shown in a previous study (Ly et al., 2014). Fig. S6. Distributions of CIPs in different types of oral samples. (A) Relative abundance of CIPs (y-axis) in dental plaque of periodontal health (PHP) and disease (PDP). (B) Relative abundance of CIPs in subgingival (SUB) and supragingival (SUP) samples. Reads mapping to CIPs were counted to calculate their abundance in each sample (n = 10). The star represents the significant difference (Asterisk denotes P < 0.05, Mann-Whitney U-test). Fig. S7. Several lines of evidence that support the connections in the cross-infection network. (A) Spacers from 11 distinct reads locate on a phage contig (Supragingival_plaque_LANL_312552, 9476bp), which supports the connection between bacteria Aggregatibacter actinomycetemcomitans (Aa) and Pseudomonas stutzeri (Ps). Aa dr represents direct repeats identified from A. actinomycetemcomitans genome. Ps dr represents direct repeats identified from P. stutzeri genome. (B) Spacers supporting the connections between Streptococcus salivarius (Ss), S. infantis (Si) and S. anginosus (Sa) can be aligned to different loci of the same phage contig (C35702196_63.0_0.370, 10475bp). (C) Six distinct reads support the connection between Campylobacter gracilis and Streptococcus infantis, and Campylobacter gracilis is connected with Streptococcus mitis by another phage genome. Table S1. Samples used in this study.
istex:21995B1711292036798FC80C765F132E3B542B46
National Natural Science Foundation of China - No. 91131013; No. 31300110
ark:/67375/WNG-RS5GFQ7G-Q
ArticleID:EMI12923
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
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ISSN:1462-2912
1462-2920
1462-2920
DOI:10.1111/1462-2920.12923