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Chapter 11 : The Bacteriophages of Group A Streptococci

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Abstract:

This chapter focuses on the influence that the bacteriophages of , both lytic and lysogenic or temperate, have on the biology and dissemination of virulence factors of this important gram-positive pathogen. The lytic bacteriophages infect their specific host bacterium, replicate their genome and assemble new virions, and then rupture the host to release the newly formed phages. Lytic phages can play important roles in the shaping of the biology of their GAS hosts, through elimination of the phagesusceptible members of a population consisting of more than one strain, selection for the rare phage-resistant variants in a mostly homogenous population, or by being the vectors of genetic exchange through generalized transduction. Although the role played by lytic streptococcal phages in pathogenesis may be indirect, acting as vehicles of genetic exchange through generalized transduction, lysogeny by GAS bacteriophages can directly enhance the pathogenic potential of the host through toxigenic conversion. The allelic variation is more than would be expected to result from accumulated random mutations between genetically isolated individuals. Because transduction is the only known natural means of genetic exchange, it is likely that this mechanism and its associated bacteriophages play an important role in the genetic shifts seen in GAS. A better understanding of streptococcal transduction may prove key to understanding the flow of genetic information in natural populations of GAS and the horizontal transfer of information from other genera.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11

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Figures

Image of FIGURE 1
FIGURE 1

Bacteriophage attachment sites in the genome. The locations of the genome prophages on the genome are shown as a generalized GAS backbone based upon the M1 genome; prophages that share the same attachment site are boxed together. The rRNA operons are indicated as white blocks; the cluster of virulence genes flanking is hatched. The origin of replication is indicated ().

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Image of FIGURE 2
FIGURE 2

5′-integration of phage SF370.4 interrupts MMR. The potential for gene interruption by 5′-integration is illustrated by comparing the MMR region from strain SF370 (upper) with that from MGAS315 (lower). In strains lacking a prophage at this site, the genes for , , , , and are predicted to be expressed on a polycistronic mRNA (indicated below by a heavy arrow) with the promoter position upstream of (←). The presence of phage SF370.4 separates the and the downstream genes from and the promoter, potentially creating a polar mutation.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Image of FIGURE 3
FIGURE 3

Multiple alignment of the genome prophages of (see Table 2 ). The genomes of the major prophages found in the six completed genomes were aligned by dot plot analysis using a window size of 11. The three phages that integrate at and the transposon/phage element MGAS10394.4 were excluded from this analysis.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Image of FIGURE 4
FIGURE 4

Phylogram of the identified genome prophages. The phylogenetic tree with split decomposition analysis of the GAS genome phages shows probable groups with related evolutionary histories. Multiple sequence alignment of the prophage genomes was done using CLUSTALX ( ). Phylogenetic analysis was done using the split decomposition method ( ), and the software program SplitsTree ( ) was used to generate the final tree.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Image of FIGURE 5
FIGURE 5

The cluster of prophages sharing a conserved region with phage SF370.1. The prophages with a conserved region encompassing the late genes for the phage structural proteins are compared by dot plot analysis. The genome of phage SF370.1 is shown below with the predicted open reading frames of the conserved region shaded in gray. The integrase gene (hatched) and virulence genes (black) are positioned at the flanking ends of the prophage genome; the box below the integrase gene indicates the site of attachment for each phage in the group, and the one below the virulence genes indicates the toxin or virulence genes associated with each prophage.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Image of FIGURE 6
FIGURE 6

The prophages integrated at the histonelike protein gene. The prophages from each of the six genomes that use the histonelike gene as are aligned by dot plot analysis. The prophages are identified by the name of the GAS genome that they occupy.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Image of FIGURE 7
FIGURE 7

The MMR-converting phages. The prophages from SF370, MGAS10394, and Manfredo that integrate into the 5′ end of are compared by dot plot analysis. The open reading frames for the phages are shown flanking the plot: SF370.4 (below), Manfredo (right), and MGAS10394.8 (above) with the lysogeny (gray), replication (black), and probable regulation (white) modules indicated. Although no structure genes are present, all three prophages have identifiable and sites.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Image of FIGURE 8
FIGURE 8

() The late gene regions of the group IV prophages. Some of the identifiable genes are listed below the MGAS8232 phi SpeLM prophage genome; the corresponding color scheme is used to identify related genes in the other prophages. The locations of probable mutations are indicated by the box symbol.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Image of FIGURE 9
FIGURE 9

%G+C and codon usage of the native gene and “species-optimized” variants. (above) The %G+C plot of the native (upper) is shown compared to the plot of a reverse-translated version (lower) created using a codon table with the most frequently used codons from SF370 (window size = 40). (Next page) A multiple alignment is shown comparing the native with reverse-translated variants created with optimized codon usage from a number of bacterial species: , , , , , and Regions of identity (>25%) are shaded in gray. Reverse translation was done using a program written in PERL with species-specific codon tables.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Image of FIGURE 10
FIGURE 10

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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Tables

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TABLE 1

Prophages and major prophage remnants identified in the sequenced genomes

The complete prophage and major prophage remnants from each of the six completed GAS genomes were analyzed for the site of attachment, duplication sequence, and identifiable toxin genes or other virulence genes. In general, nomenclature used in the annotation of a genome was adopted. Since an annotation for the M6 Manfredo strain has not been yet released, a descriptive nomenclature was adopted based upon the virulence gene associated with the phage or, when lacking such a gene, the site of phage attachment.

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
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TABLE 2

Key to Fig. 3

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11
Generic image for table
TABLE 3

Key to Fig. 4

Citation: McShan W. 2006. The Bacteriophages of Group A Streptococci, p 123-142. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch11

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