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Identification of the pangenome and its components in 14 distinct Aggregatibacter actinomycetemcomitans strains by comparative genomic analysis.

Kittichotirat W, Bumgarner RE, Asikainen S, Chen C - PLoS ONE (2011)

Bottom Line: The genomic differences were occasionally greater for strains of the same serotypes than strains of different serotypes.Cumulatively, 777 strain-specific genes were found on these islands and represented 61% of the flexible gene pool.Moreover, the genomic variation within each clonal lineage of A. actinomycetemcomitans (as defined by serotype grouping) may be greater than between clonal lineages.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology, University of Washington, Seattle, Washington, United States of America.

ABSTRACT

Background: Aggregatibacter actinomycetemcomitans is genetically heterogeneous and comprises distinct clonal lineages that may have different virulence potentials. However, limited information of the strain-to-strain genomic variations is available.

Methodology/principal findings: The genome sequences of 11 A. actinomycetemcomitans strains (serotypes a-f) were generated de novo, annotated and combined with three previously sequenced genomes (serotypes a-c) for comparative genomic analysis. Two major groups were identified; serotypes a, d, e, and f, and serotypes b and c. A serotype e strain was found to be distinct from both groups. The size of the pangenome was 3,301 genes, which included 2,034 core genes and 1,267 flexible genes. The number of core genes is estimated to stabilize at 2,060, while the size of the pangenome is estimated to increase by 16 genes with every additional strain sequenced in the future. Within each strain 16.7-29.4% of the genome belonged to the flexible gene pool. Between any two strains 0.4-19.5% of the genomes were different. The genomic differences were occasionally greater for strains of the same serotypes than strains of different serotypes. Furthermore, 171 genomic islands were identified. Cumulatively, 777 strain-specific genes were found on these islands and represented 61% of the flexible gene pool.

Conclusions/significance: Substantial genomic differences were detected among A. actinomycetemcomitans strains. Genomic islands account for more than half of the flexible genes. The phenotype and virulence of A. actinomycetemcomitans may not be defined by any single strain. Moreover, the genomic variation within each clonal lineage of A. actinomycetemcomitans (as defined by serotype grouping) may be greater than between clonal lineages. The large genomic data set in this study will be useful to further examine the molecular basis of variable virulence among A. actinomycetemcomitans strains.

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Related in: MedlinePlus

Pair-wise genomic comparisons among A. actinomycetemcomitans strains.A heat map of the genome variation among 14 A. actinomycetemcomitans strains is shown. The numbers in the box show the % of protein-coding genes found in one genome (left) but not another. The data are organized by serotypes; a (D17P3, D7S-1, and H5P-1), d (I63B), e (SC1083), e (SCC393), f (D18P1), b (HK1651, ANH9381, SCC1398, I23C), c (D11S-1, D17P2, SCC2302). The patterns of genome similarity mirror those found in phylogenetic analysis by 16S rRNA gene sequences or 25 housekeeping genes shown in Figures 1 and 2. The numbers in parenthesis on the left of the map indicate the numbers of protein-coding genes.
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pone-0022420-g004: Pair-wise genomic comparisons among A. actinomycetemcomitans strains.A heat map of the genome variation among 14 A. actinomycetemcomitans strains is shown. The numbers in the box show the % of protein-coding genes found in one genome (left) but not another. The data are organized by serotypes; a (D17P3, D7S-1, and H5P-1), d (I63B), e (SC1083), e (SCC393), f (D18P1), b (HK1651, ANH9381, SCC1398, I23C), c (D11S-1, D17P2, SCC2302). The patterns of genome similarity mirror those found in phylogenetic analysis by 16S rRNA gene sequences or 25 housekeeping genes shown in Figures 1 and 2. The numbers in parenthesis on the left of the map indicate the numbers of protein-coding genes.

Mentions: Figure 4 provides a summary of strain-to-strain comparisons of protein-coding genes of the genomes. Depending on the pair of strains compared and the direction of the comparison, the percentage of genes present in one genome but not in another ranged from 0.4% to 19.5%. Two groups of strains were recognized based on the similarity matrix. One group was formed by the strains of serotypes a, d, e (except strain SC1083) and f. The other group was formed by the strains of serotypes b and c. The serotype e strain SC1083 did not seem to follow the pattern. Two-way hierarchical clustering analysis of the flexible genes also illustrated the same patterns of two major groups and the distinctiveness of strain SC1083 (Figure 5). The segregation in the pattern of genomic variation among strains mirrored that found in phylogenetic analysis using housekeeping genes (Figure 1).


Identification of the pangenome and its components in 14 distinct Aggregatibacter actinomycetemcomitans strains by comparative genomic analysis.

Kittichotirat W, Bumgarner RE, Asikainen S, Chen C - PLoS ONE (2011)

Pair-wise genomic comparisons among A. actinomycetemcomitans strains.A heat map of the genome variation among 14 A. actinomycetemcomitans strains is shown. The numbers in the box show the % of protein-coding genes found in one genome (left) but not another. The data are organized by serotypes; a (D17P3, D7S-1, and H5P-1), d (I63B), e (SC1083), e (SCC393), f (D18P1), b (HK1651, ANH9381, SCC1398, I23C), c (D11S-1, D17P2, SCC2302). The patterns of genome similarity mirror those found in phylogenetic analysis by 16S rRNA gene sequences or 25 housekeeping genes shown in Figures 1 and 2. The numbers in parenthesis on the left of the map indicate the numbers of protein-coding genes.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3139650&req=5

pone-0022420-g004: Pair-wise genomic comparisons among A. actinomycetemcomitans strains.A heat map of the genome variation among 14 A. actinomycetemcomitans strains is shown. The numbers in the box show the % of protein-coding genes found in one genome (left) but not another. The data are organized by serotypes; a (D17P3, D7S-1, and H5P-1), d (I63B), e (SC1083), e (SCC393), f (D18P1), b (HK1651, ANH9381, SCC1398, I23C), c (D11S-1, D17P2, SCC2302). The patterns of genome similarity mirror those found in phylogenetic analysis by 16S rRNA gene sequences or 25 housekeeping genes shown in Figures 1 and 2. The numbers in parenthesis on the left of the map indicate the numbers of protein-coding genes.
Mentions: Figure 4 provides a summary of strain-to-strain comparisons of protein-coding genes of the genomes. Depending on the pair of strains compared and the direction of the comparison, the percentage of genes present in one genome but not in another ranged from 0.4% to 19.5%. Two groups of strains were recognized based on the similarity matrix. One group was formed by the strains of serotypes a, d, e (except strain SC1083) and f. The other group was formed by the strains of serotypes b and c. The serotype e strain SC1083 did not seem to follow the pattern. Two-way hierarchical clustering analysis of the flexible genes also illustrated the same patterns of two major groups and the distinctiveness of strain SC1083 (Figure 5). The segregation in the pattern of genomic variation among strains mirrored that found in phylogenetic analysis using housekeeping genes (Figure 1).

Bottom Line: The genomic differences were occasionally greater for strains of the same serotypes than strains of different serotypes.Cumulatively, 777 strain-specific genes were found on these islands and represented 61% of the flexible gene pool.Moreover, the genomic variation within each clonal lineage of A. actinomycetemcomitans (as defined by serotype grouping) may be greater than between clonal lineages.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology, University of Washington, Seattle, Washington, United States of America.

ABSTRACT

Background: Aggregatibacter actinomycetemcomitans is genetically heterogeneous and comprises distinct clonal lineages that may have different virulence potentials. However, limited information of the strain-to-strain genomic variations is available.

Methodology/principal findings: The genome sequences of 11 A. actinomycetemcomitans strains (serotypes a-f) were generated de novo, annotated and combined with three previously sequenced genomes (serotypes a-c) for comparative genomic analysis. Two major groups were identified; serotypes a, d, e, and f, and serotypes b and c. A serotype e strain was found to be distinct from both groups. The size of the pangenome was 3,301 genes, which included 2,034 core genes and 1,267 flexible genes. The number of core genes is estimated to stabilize at 2,060, while the size of the pangenome is estimated to increase by 16 genes with every additional strain sequenced in the future. Within each strain 16.7-29.4% of the genome belonged to the flexible gene pool. Between any two strains 0.4-19.5% of the genomes were different. The genomic differences were occasionally greater for strains of the same serotypes than strains of different serotypes. Furthermore, 171 genomic islands were identified. Cumulatively, 777 strain-specific genes were found on these islands and represented 61% of the flexible gene pool.

Conclusions/significance: Substantial genomic differences were detected among A. actinomycetemcomitans strains. Genomic islands account for more than half of the flexible genes. The phenotype and virulence of A. actinomycetemcomitans may not be defined by any single strain. Moreover, the genomic variation within each clonal lineage of A. actinomycetemcomitans (as defined by serotype grouping) may be greater than between clonal lineages. The large genomic data set in this study will be useful to further examine the molecular basis of variable virulence among A. actinomycetemcomitans strains.

Show MeSH
Related in: MedlinePlus