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Composite mobile genetic elements disseminating macrolide resistance in Streptococcus pneumoniae.

Chancey ST, Agrawal S, Schroeder MR, Farley MM, Tettelin H, Stephens DS - Front Microbiol (2015)

Bottom Line: The results reported here include identification of novel insertion sites for Mega and characterization of the insertion sites of Tn916-like elements in the pneumococcal chromosome and in larger composite elements.The data indicate that integration of elements by conjugation was infrequent compared to recombination.Thus, it appears that conjugative mobile elements allow the pneumococcus to acquire DNA from distantly related bacteria, but once integrated into a pneumococcal genome, transformation and recombination is the primary mechanism for transmission of novel DNA throughout the pneumococcal population.

View Article: PubMed Central - PubMed

Affiliation: Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine Atlanta, GA, USA ; Laboratories of Microbial Pathogenesis, Department of Veterans Affairs Medical Center Atlanta, GA, USA.

ABSTRACT
Macrolide resistance in Streptococcus pneumoniae emerged in the U.S. and globally during the early 1990's. The RNA methylase encoded by erm(B) and the macrolide efflux genes mef(E) and mel were identified as the resistance determining factors. These genes are disseminated in the pneumococcus on mobile, often chimeric elements consisting of multiple smaller elements. To better understand the variety of elements encoding macrolide resistance and how they have evolved in the pre- and post-conjugate vaccine eras, the genomes of 121 invasive and ten carriage isolates from Atlanta from 1994 to 2011 were analyzed for mobile elements involved in the dissemination of macrolide resistance. The isolates were selected to provide broad coverage of the genetic variability of antibiotic resistant pneumococci and included 100 invasive isolates resistant to macrolides. Tn916-like elements carrying mef(E) and mel on the Macrolide Genetic Assembly (Mega) and erm(B) on the erm(B) element and Tn917 were integrated into the pneumococcal chromosome backbone and into larger Tn5253-like composite elements. The results reported here include identification of novel insertion sites for Mega and characterization of the insertion sites of Tn916-like elements in the pneumococcal chromosome and in larger composite elements. The data indicate that integration of elements by conjugation was infrequent compared to recombination. Thus, it appears that conjugative mobile elements allow the pneumococcus to acquire DNA from distantly related bacteria, but once integrated into a pneumococcal genome, transformation and recombination is the primary mechanism for transmission of novel DNA throughout the pneumococcal population.

No MeSH data available.


Related in: MedlinePlus

Whole genome SNP-derived phylogenetic tree. Whole genome single nucleotide polymorphism analysis of 166 genomes, including 147 from the present study and nine publically available closed genomes, using the TIGR4 genome as reference. The tree was rooted using S. infantis SPAR10 as the outgroup. Numbers on the perimeter indicate the MLST clonal complex of the isolates and are colored the same as the branches leading to the isolates in each complex. The clonal complex of each sequence type was defined as the founder ST of a clonal group, as predicted by eBURST analyses of the entire S. pneumoniae MLST databased accessed in September, 2014 (http://pubmlst.org/spneumoniae/). Isolate names and serotype labels colored blue indicates that the strain was isolated prior to the introduction of PCV7 in 2000. Red colored names and serotypes indicate the strains were isolated in 2000 or later. Colored dots indicate a Mega insertion in the isolate and are color coded by Mega insertion site, light blue, class I; dark blue, class II; red, class III; pink, class IV; green, class V (Tn916 orf6); and gold, novel insertion site.
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Figure 2: Whole genome SNP-derived phylogenetic tree. Whole genome single nucleotide polymorphism analysis of 166 genomes, including 147 from the present study and nine publically available closed genomes, using the TIGR4 genome as reference. The tree was rooted using S. infantis SPAR10 as the outgroup. Numbers on the perimeter indicate the MLST clonal complex of the isolates and are colored the same as the branches leading to the isolates in each complex. The clonal complex of each sequence type was defined as the founder ST of a clonal group, as predicted by eBURST analyses of the entire S. pneumoniae MLST databased accessed in September, 2014 (http://pubmlst.org/spneumoniae/). Isolate names and serotype labels colored blue indicates that the strain was isolated prior to the introduction of PCV7 in 2000. Red colored names and serotypes indicate the strains were isolated in 2000 or later. Colored dots indicate a Mega insertion in the isolate and are color coded by Mega insertion site, light blue, class I; dark blue, class II; red, class III; pink, class IV; green, class V (Tn916 orf6); and gold, novel insertion site.

Mentions: The 147 isolates from this study and 15 publically available genomes were compared using whole genome single nucleotide polymorphism (SNP) analyses. The resulting phylogenetic tree is shown in Figure 2. The genomes clustered into MLST clonal complexes with the exception of CC156 which was divided into three clades (Figure 2). This may be an example of a limitation of MLST typing as the three clusters appear to be unrelated. CC156 is a large complex consisting of multiple subgroups thus not all were as closely related as the label CC156 implied (Figure S1). For example ST90 has only one allele in common with ST156. However, it was interesting to observe that two of the CC156 subgroups appear to be linked by a common Mega insertion event (see below). Further, the eBURST-predicted subgroups (SG90, SG124 and SG156) are well-established independent clonal complexes (CC90, CC124 and CC156, respectively) indicating that their inclusion into a single clonal complex is an artifact of eBURST and not a true indication of common ancestry.


Composite mobile genetic elements disseminating macrolide resistance in Streptococcus pneumoniae.

Chancey ST, Agrawal S, Schroeder MR, Farley MM, Tettelin H, Stephens DS - Front Microbiol (2015)

Whole genome SNP-derived phylogenetic tree. Whole genome single nucleotide polymorphism analysis of 166 genomes, including 147 from the present study and nine publically available closed genomes, using the TIGR4 genome as reference. The tree was rooted using S. infantis SPAR10 as the outgroup. Numbers on the perimeter indicate the MLST clonal complex of the isolates and are colored the same as the branches leading to the isolates in each complex. The clonal complex of each sequence type was defined as the founder ST of a clonal group, as predicted by eBURST analyses of the entire S. pneumoniae MLST databased accessed in September, 2014 (http://pubmlst.org/spneumoniae/). Isolate names and serotype labels colored blue indicates that the strain was isolated prior to the introduction of PCV7 in 2000. Red colored names and serotypes indicate the strains were isolated in 2000 or later. Colored dots indicate a Mega insertion in the isolate and are color coded by Mega insertion site, light blue, class I; dark blue, class II; red, class III; pink, class IV; green, class V (Tn916 orf6); and gold, novel insertion site.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4321634&req=5

Figure 2: Whole genome SNP-derived phylogenetic tree. Whole genome single nucleotide polymorphism analysis of 166 genomes, including 147 from the present study and nine publically available closed genomes, using the TIGR4 genome as reference. The tree was rooted using S. infantis SPAR10 as the outgroup. Numbers on the perimeter indicate the MLST clonal complex of the isolates and are colored the same as the branches leading to the isolates in each complex. The clonal complex of each sequence type was defined as the founder ST of a clonal group, as predicted by eBURST analyses of the entire S. pneumoniae MLST databased accessed in September, 2014 (http://pubmlst.org/spneumoniae/). Isolate names and serotype labels colored blue indicates that the strain was isolated prior to the introduction of PCV7 in 2000. Red colored names and serotypes indicate the strains were isolated in 2000 or later. Colored dots indicate a Mega insertion in the isolate and are color coded by Mega insertion site, light blue, class I; dark blue, class II; red, class III; pink, class IV; green, class V (Tn916 orf6); and gold, novel insertion site.
Mentions: The 147 isolates from this study and 15 publically available genomes were compared using whole genome single nucleotide polymorphism (SNP) analyses. The resulting phylogenetic tree is shown in Figure 2. The genomes clustered into MLST clonal complexes with the exception of CC156 which was divided into three clades (Figure 2). This may be an example of a limitation of MLST typing as the three clusters appear to be unrelated. CC156 is a large complex consisting of multiple subgroups thus not all were as closely related as the label CC156 implied (Figure S1). For example ST90 has only one allele in common with ST156. However, it was interesting to observe that two of the CC156 subgroups appear to be linked by a common Mega insertion event (see below). Further, the eBURST-predicted subgroups (SG90, SG124 and SG156) are well-established independent clonal complexes (CC90, CC124 and CC156, respectively) indicating that their inclusion into a single clonal complex is an artifact of eBURST and not a true indication of common ancestry.

Bottom Line: The results reported here include identification of novel insertion sites for Mega and characterization of the insertion sites of Tn916-like elements in the pneumococcal chromosome and in larger composite elements.The data indicate that integration of elements by conjugation was infrequent compared to recombination.Thus, it appears that conjugative mobile elements allow the pneumococcus to acquire DNA from distantly related bacteria, but once integrated into a pneumococcal genome, transformation and recombination is the primary mechanism for transmission of novel DNA throughout the pneumococcal population.

View Article: PubMed Central - PubMed

Affiliation: Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine Atlanta, GA, USA ; Laboratories of Microbial Pathogenesis, Department of Veterans Affairs Medical Center Atlanta, GA, USA.

ABSTRACT
Macrolide resistance in Streptococcus pneumoniae emerged in the U.S. and globally during the early 1990's. The RNA methylase encoded by erm(B) and the macrolide efflux genes mef(E) and mel were identified as the resistance determining factors. These genes are disseminated in the pneumococcus on mobile, often chimeric elements consisting of multiple smaller elements. To better understand the variety of elements encoding macrolide resistance and how they have evolved in the pre- and post-conjugate vaccine eras, the genomes of 121 invasive and ten carriage isolates from Atlanta from 1994 to 2011 were analyzed for mobile elements involved in the dissemination of macrolide resistance. The isolates were selected to provide broad coverage of the genetic variability of antibiotic resistant pneumococci and included 100 invasive isolates resistant to macrolides. Tn916-like elements carrying mef(E) and mel on the Macrolide Genetic Assembly (Mega) and erm(B) on the erm(B) element and Tn917 were integrated into the pneumococcal chromosome backbone and into larger Tn5253-like composite elements. The results reported here include identification of novel insertion sites for Mega and characterization of the insertion sites of Tn916-like elements in the pneumococcal chromosome and in larger composite elements. The data indicate that integration of elements by conjugation was infrequent compared to recombination. Thus, it appears that conjugative mobile elements allow the pneumococcus to acquire DNA from distantly related bacteria, but once integrated into a pneumococcal genome, transformation and recombination is the primary mechanism for transmission of novel DNA throughout the pneumococcal population.

No MeSH data available.


Related in: MedlinePlus