Comparative Genomics of Recent Shiga Toxin-Producing <named-content content-type="genus-species">Escherichia coli</named-content> O104:H4: Short-Term Evolution of an Emerging Pathogen
ABSTRACT The large outbreak of diarrhea and hemolytic uremic syndrome (HUS) caused by Shiga toxin-producing Escherichia coli O104:H4 in Europe from May to July 2011 highlighted the potential of a rarely identified E. coli serogroup to cause severe disease. Prior to the outbreak, there were very few...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2013-03-01
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| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00452-12 |
| _version_ | 1818740155607941120 |
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| author | Yonatan H. Grad Paul Godfrey Gustavo C. Cerquiera Patricia Mariani-Kurkdjian Malika Gouali Edouard Bingen Terrence P. Shea Brian J. Haas Allison Griggs Sarah Young Qiandong Zeng Marc Lipsitch Matthew K. Waldor François-Xavier Weill Jennifer R. Wortman William P. Hanage |
| author_facet | Yonatan H. Grad Paul Godfrey Gustavo C. Cerquiera Patricia Mariani-Kurkdjian Malika Gouali Edouard Bingen Terrence P. Shea Brian J. Haas Allison Griggs Sarah Young Qiandong Zeng Marc Lipsitch Matthew K. Waldor François-Xavier Weill Jennifer R. Wortman William P. Hanage |
| author_sort | Yonatan H. Grad |
| collection | DOAJ |
| description | ABSTRACT The large outbreak of diarrhea and hemolytic uremic syndrome (HUS) caused by Shiga toxin-producing Escherichia coli O104:H4 in Europe from May to July 2011 highlighted the potential of a rarely identified E. coli serogroup to cause severe disease. Prior to the outbreak, there were very few reports of disease caused by this pathogen and thus little known of its diversity and evolution. The identification of cases of HUS caused by E. coli O104:H4 in France and Turkey after the outbreak and with no clear epidemiological links raises questions about whether these sporadic cases are derived from the outbreak. Here, we report genome sequences of five independent isolates from these cases and results of a comparative analysis with historical and 2011 outbreak isolates. These analyses revealed that the five isolates are not derived from the outbreak strain; however, they are more closely related to the outbreak strain and each other than to isolates identified prior to the 2011 outbreak. Over the short time scale represented by these closely related organisms, the majority of genome variation is found within their mobile genetic elements: none of the nine O104:H4 isolates compared here contain the same set of plasmids, and their prophages and genomic islands also differ. Moreover, the presence of closely related HUS-associated E. coli O104:H4 isolates supports the contention that fully virulent O104:H4 isolates are widespread and emphasizes the possibility of future food-borne E. coli O104:H4 outbreaks. IMPORTANCE In the summer of 2011, a large outbreak of bloody diarrhea with a high rate of severe complications took place in Europe, caused by a previously rarely seen Escherichia coli strain of serogroup O104:H4. Identification of subsequent infections caused by E. coli O104:H4 raised questions about whether these new cases represented ongoing transmission of the outbreak strain. In this study, we sequenced the genomes of isolates from five recent cases and compared them with historical isolates. The analyses reveal that, in the very short term, evolution of the bacterial genome takes place in parts of the genome that are exchanged among bacteria, and these regions contain genes involved in adaptation to local environments. We show that these recent isolates are not derived from the outbreak strain but are very closely related and share many of the same disease-causing genes, emphasizing the concern that these bacteria may cause future severe outbreaks. |
| first_indexed | 2024-12-18T01:36:14Z |
| format | Article |
| id | doaj.art-38df8f5dfbdb4d4fb4c6c484e68905f5 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T01:36:14Z |
| publishDate | 2013-03-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-38df8f5dfbdb4d4fb4c6c484e68905f52022-12-21T21:25:26ZengAmerican Society for MicrobiologymBio2150-75112013-03-014110.1128/mBio.00452-12Comparative Genomics of Recent Shiga Toxin-Producing <named-content content-type="genus-species">Escherichia coli</named-content> O104:H4: Short-Term Evolution of an Emerging PathogenYonatan H. Grad0Paul Godfrey1Gustavo C. Cerquiera2Patricia Mariani-Kurkdjian3Malika Gouali4Edouard Bingen5Terrence P. Shea6Brian J. Haas7Allison Griggs8Sarah Young9Qiandong Zeng10Marc Lipsitch11Matthew K. Waldor12François-Xavier Weill13Jennifer R. Wortman14William P. Hanage15Department of Medicine, Brigham and Women’s Hospital, Boston, Massachusetts, USABroad Institute of Harvard and MIT, Cambridge, Massachusetts, USABroad Institute of Harvard and MIT, Cambridge, Massachusetts, USALaboratoire Associé au Centre National de Référence des Escherichia coli et Shigella, Service de Microbiologie, Hôpital Robert Debré, Assistance Publique-Hôpitaux de Paris, Paris, FranceInstitut Pasteur, Unité des Bactéries Pathogènes Entériques, Centre National de Référence des Escherichia coli et Shigella, Paris, FranceLaboratoire Associé au Centre National de Référence des Escherichia coli et Shigella, Service de Microbiologie, Hôpital Robert Debré, Assistance Publique-Hôpitaux de Paris, Paris, FranceBroad Institute of Harvard and MIT, Cambridge, Massachusetts, USABroad Institute of Harvard and MIT, Cambridge, Massachusetts, USABroad Institute of Harvard and MIT, Cambridge, Massachusetts, USABroad Institute of Harvard and MIT, Cambridge, Massachusetts, USABroad Institute of Harvard and MIT, Cambridge, Massachusetts, USADepartment of Epidemiology, Center for Communicable Disease Dynamics, Harvard School of Public Health, Boston, Massachusetts, USADepartment of Medicine, Brigham and Women’s Hospital, Boston, Massachusetts, USAInstitut Pasteur, Unité des Bactéries Pathogènes Entériques, Centre National de Référence des Escherichia coli et Shigella, Paris, FranceBroad Institute of Harvard and MIT, Cambridge, Massachusetts, USADepartment of Epidemiology, Center for Communicable Disease Dynamics, Harvard School of Public Health, Boston, Massachusetts, USAABSTRACT The large outbreak of diarrhea and hemolytic uremic syndrome (HUS) caused by Shiga toxin-producing Escherichia coli O104:H4 in Europe from May to July 2011 highlighted the potential of a rarely identified E. coli serogroup to cause severe disease. Prior to the outbreak, there were very few reports of disease caused by this pathogen and thus little known of its diversity and evolution. The identification of cases of HUS caused by E. coli O104:H4 in France and Turkey after the outbreak and with no clear epidemiological links raises questions about whether these sporadic cases are derived from the outbreak. Here, we report genome sequences of five independent isolates from these cases and results of a comparative analysis with historical and 2011 outbreak isolates. These analyses revealed that the five isolates are not derived from the outbreak strain; however, they are more closely related to the outbreak strain and each other than to isolates identified prior to the 2011 outbreak. Over the short time scale represented by these closely related organisms, the majority of genome variation is found within their mobile genetic elements: none of the nine O104:H4 isolates compared here contain the same set of plasmids, and their prophages and genomic islands also differ. Moreover, the presence of closely related HUS-associated E. coli O104:H4 isolates supports the contention that fully virulent O104:H4 isolates are widespread and emphasizes the possibility of future food-borne E. coli O104:H4 outbreaks. IMPORTANCE In the summer of 2011, a large outbreak of bloody diarrhea with a high rate of severe complications took place in Europe, caused by a previously rarely seen Escherichia coli strain of serogroup O104:H4. Identification of subsequent infections caused by E. coli O104:H4 raised questions about whether these new cases represented ongoing transmission of the outbreak strain. In this study, we sequenced the genomes of isolates from five recent cases and compared them with historical isolates. The analyses reveal that, in the very short term, evolution of the bacterial genome takes place in parts of the genome that are exchanged among bacteria, and these regions contain genes involved in adaptation to local environments. We show that these recent isolates are not derived from the outbreak strain but are very closely related and share many of the same disease-causing genes, emphasizing the concern that these bacteria may cause future severe outbreaks.https://journals.asm.org/doi/10.1128/mBio.00452-12 |
| spellingShingle | Yonatan H. Grad Paul Godfrey Gustavo C. Cerquiera Patricia Mariani-Kurkdjian Malika Gouali Edouard Bingen Terrence P. Shea Brian J. Haas Allison Griggs Sarah Young Qiandong Zeng Marc Lipsitch Matthew K. Waldor François-Xavier Weill Jennifer R. Wortman William P. Hanage Comparative Genomics of Recent Shiga Toxin-Producing <named-content content-type="genus-species">Escherichia coli</named-content> O104:H4: Short-Term Evolution of an Emerging Pathogen mBio |
| title | Comparative Genomics of Recent Shiga Toxin-Producing <named-content content-type="genus-species">Escherichia coli</named-content> O104:H4: Short-Term Evolution of an Emerging Pathogen |
| title_full | Comparative Genomics of Recent Shiga Toxin-Producing <named-content content-type="genus-species">Escherichia coli</named-content> O104:H4: Short-Term Evolution of an Emerging Pathogen |
| title_fullStr | Comparative Genomics of Recent Shiga Toxin-Producing <named-content content-type="genus-species">Escherichia coli</named-content> O104:H4: Short-Term Evolution of an Emerging Pathogen |
| title_full_unstemmed | Comparative Genomics of Recent Shiga Toxin-Producing <named-content content-type="genus-species">Escherichia coli</named-content> O104:H4: Short-Term Evolution of an Emerging Pathogen |
| title_short | Comparative Genomics of Recent Shiga Toxin-Producing <named-content content-type="genus-species">Escherichia coli</named-content> O104:H4: Short-Term Evolution of an Emerging Pathogen |
| title_sort | comparative genomics of recent shiga toxin producing named content content type genus species escherichia coli named content o104 h4 short term evolution of an emerging pathogen |
| url | https://journals.asm.org/doi/10.1128/mBio.00452-12 |
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