Genome Res. 13:1042-1055, 2003
©2003 by Cold Spring Harbor Laboratory Press; ISSN 1088-9051/03 $5.00
Genome Sequence of an M3 Strain of Streptococcus pyogenes Reveals a Large-Scale Genomic Rearrangement in Invasive Strains and New Insights into Phage Evolution
Ichiro Nakagawa1,7,
Ken Kurokawa2,
Atsushi Yamashita3,
Masanobu Nakata1,
Yusuke Tomiyasu1,
Nobuo Okahashi1,
Shigetada Kawabata1,4,
Kiyoshi Yamazaki2,
Tadayoshi Shiba5,
Teruo Yasunaga2,
Hideo Hayashi6,
Masahira Hattori3 and
Shigeyuki Hamada1
1 Department of Oral and Molecular Microbiology, Osaka University Graduate School of Dentistry, Suita-Osaka 565-0871, Japan
2 Genome Information Research Center, Osaka University, Suita-Osaka 565-0871, Japan
3 Kitasato Institute for Life Sciences, Kitasato University, Sagamihara-Kanagawa 228-8555, Japan
4 PRESTO, Japan Science and Technology Corporation, Kawaguchi, Saitama 332-0012, Japan
5 School of Science, Kitasato University, Sagamihara-Kanagawa 228-8555, Japan
6 Institute of Basic Medical Sciences, University of Tsukuba, Tsukuba-Ibaraki 305-8575, Japan
Group Astreptococcus (GAS) is a gram-positive bacterial pathogen that causes various suppurative infections and nonsuppurative sequelae. Since the late 1980s, streptococcal toxic-shock like syndrome (STSS) and severe invasive GAS infections have been reported globally. Here we sequenced the genome of serotype M3 strain SSI-1, isolated from an STSS patient in Japan, and compared it with those of other GAS strains. The SSI-1 genome is composed of 1,884,275 bp, and 1.7 Mb of the sequence is highly conserved relative to strain SF370 (serotype M1) and MGAS8232 (serotype M18), and almost completely conserved relative to strain MGAS315 (serotype M3). However, a large genomic rearrangement has been shown to occur across the replication axis between the homologous rrn-comX1 regions and between two prophage-coding regions across the replication axis. Atotal of 1 Mb of chromosomal DNA is inverted across the replication axis. Interestingly, the recombinations between the prophage regions are within the phage genes, and the genes encoding superantigens and mitogenic factors are interchanged between two prophages. This genomic rearrangement occurs in 65% of clinical isolates (64/94) collected after 1990, whereas it is found in only 25% of clinical isolates (7/28) collected before 1985. These observations indicate that streptococcal phages represent important plasticity regions in the GAS chromosome where recombination between homologous phage genes can occur and result not only in new phage derivatives, but also in large chromosomal rearrangements.
Article and publication are at http://www.genome.org/cgi/doi/10.1101/gr.1096703.
7 Corresponding author. E-MAIL ichiro{at}dent.osaka-u.ac.jp; FAX +81-6-6878-4755.
[Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to DDBJ under accession no. BA000034. The following individuals kindly provided reagents, samples, or unpublished information as indicated in the paper: K. Kikuchi, S. Murai, M. Ohta, T. Ikebe, and H. Watanabe.]

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|
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|

|
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|
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|
 |
|

|
 |

|
 |
 
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|
 |
|

|
 |

|
 |
 
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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187(12):
4163 - 4172.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Lerat and H. Ochman
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33(10):
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[Abstract]
[Full Text]
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|
 |
|

|
 |

|
 |
 
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15(6):
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. K. Aziz, R. A. Edwards, W. W. Taylor, D. E. Low, A. McGeer, and M. Kotb
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J. Bacteriol.,
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187(10):
3311 - 3318.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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February 1, 2005;
102(5):
1679 - 1684.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Lindahl, M. Stalhammar-Carlemalm, and T. Areschoug
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18(1):
102 - 127.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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J. Biol. Chem.,
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279(44):
45909 - 45918.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Brussow, C. Canchaya, and W.-D. Hardt
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Microbiol. Mol. Biol. Rev.,
September 1, 2004;
68(3):
560 - 602.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. B. Beres, G. L. Sylva, D. E. Sturdevant, C. N. Granville, M. Liu, S. M. Ricklefs, A. R. Whitney, L. D. Parkins, N. P. Hoe, G. J. Adams, et al.
Genome-wide molecular dissection of serotype M3 group A Streptococcus strains causing two epidemics of invasive infections
PNAS,
August 10, 2004;
101(32):
11833 - 11838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. M. Huang, M. Robertson, J. Aron, and S. Casjens
Telomere Exchange between Linear Replicons of Borrelia burgdorferi
J. Bacteriol.,
July 1, 2004;
186(13):
4134 - 4141.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. DeShazer
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J. Bacteriol.,
June 15, 2004;
186(12):
3938 - 3950.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kalia and D. E. Bessen
Natural Selection and Evolution of Streptococcal Virulence Genes Involved in Tissue-Specific Adaptations
J. Bacteriol.,
January 1, 2004;
186(1):
110 - 121.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|