Prospective Genomic Characterization of the German Enterohemorrhagic Escherichia coli O104:H4 Outbreak by Rapid Next Generation Sequencing Technology
An ongoing outbreak of exceptionally virulent Shiga toxin (Stx)-producing Escherichia coli O104:H4 centered in Germany, has caused over 830 cases of hemolytic uremic syndrome (HUS) and 46 deaths since May 2011. Serotype O104:H4, which has not been detected in animals, has rarely been associated with...
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| Published in | PloS one Vol. 6; no. 7; p. e22751 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
20.07.2011
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0022751 |
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| Abstract | An ongoing outbreak of exceptionally virulent Shiga toxin (Stx)-producing Escherichia coli O104:H4 centered in Germany, has caused over 830 cases of hemolytic uremic syndrome (HUS) and 46 deaths since May 2011. Serotype O104:H4, which has not been detected in animals, has rarely been associated with HUS in the past. To prospectively elucidate the unique characteristics of this strain in the early stages of this outbreak, we applied whole genome sequencing on the Life Technologies Ion Torrent PGM™ sequencer and Optical Mapping to characterize one outbreak isolate (LB226692) and a historic O104:H4 HUS isolate from 2001 (01-09591). Reference guided draft assemblies of both strains were completed with the newly introduced PGM™ within 62 hours. The HUS-associated strains both carried genes typically found in two types of pathogenic E. coli, enteroaggregative E. coli (EAEC) and enterohemorrhagic E. coli (EHEC). Phylogenetic analyses of 1,144 core E. coli genes indicate that the HUS-causing O104:H4 strains and the previously published sequence of the EAEC strain 55989 show a close relationship but are only distantly related to common EHEC serotypes. Though closely related, the outbreak strain differs from the 2001 strain in plasmid content and fimbrial genes. We propose a model in which EAEC 55989 and EHEC O104:H4 strains evolved from a common EHEC O104:H4 progenitor, and suggest that by stepwise gain and loss of chromosomal and plasmid-encoded virulence factors, a highly pathogenic hybrid of EAEC and EHEC emerged as the current outbreak clone. In conclusion, rapid next-generation technologies facilitated prospective whole genome characterization in the early stages of an outbreak. |
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| AbstractList | An ongoing outbreak of exceptionally virulent Shiga toxin (Stx)-producing Escherichia coli O104:H4 centered in Germany, has caused over 830 cases of hemolytic uremic syndrome (HUS) and 46 deaths since May 2011. Serotype O104:H4, which has not been detected in animals, has rarely been associated with HUS in the past. To prospectively elucidate the unique characteristics of this strain in the early stages of this outbreak, we applied whole genome sequencing on the Life Technologies Ion Torrent PGM™ sequencer and Optical Mapping to characterize one outbreak isolate (LB226692) and a historic O104:H4 HUS isolate from 2001 (01-09591). Reference guided draft assemblies of both strains were completed with the newly introduced PGM™ within 62 hours. The HUS-associated strains both carried genes typically found in two types of pathogenic E. coli, enteroaggregative E. coli (EAEC) and enterohemorrhagic E. coli (EHEC). Phylogenetic analyses of 1,144 core E. coli genes indicate that the HUS-causing O104:H4 strains and the previously published sequence of the EAEC strain 55989 show a close relationship but are only distantly related to common EHEC serotypes. Though closely related, the outbreak strain differs from the 2001 strain in plasmid content and fimbrial genes. We propose a model in which EAEC 55989 and EHEC O104:H4 strains evolved from a common EHEC O104:H4 progenitor, and suggest that by stepwise gain and loss of chromosomal and plasmid-encoded virulence factors, a highly pathogenic hybrid of EAEC and EHEC emerged as the current outbreak clone. In conclusion, rapid next-generation technologies facilitated prospective whole genome characterization in the early stages of an outbreak. An ongoing outbreak of exceptionally virulent Shiga toxin (Stx)-producing Escherichia coli O104:H4 centered in Germany, has caused over 830 cases of hemolytic uremic syndrome (HUS) and 46 deaths since May 2011. Serotype O104:H4, which has not been detected in animals, has rarely been associated with HUS in the past. To prospectively elucidate the unique characteristics of this strain in the early stages of this outbreak, we applied whole genome sequencing on the Life Technologies Ion Torrent PGM[TM] sequencer and Optical Mapping to characterize one outbreak isolate (LB226692) and a historic O104:H4 HUS isolate from 2001 (01-09591). Reference guided draft assemblies of both strains were completed with the newly introduced PGM[TM] within 62 hours. The HUS-associated strains both carried genes typically found in two types of pathogenic E. coli, enteroaggregative E. coli (EAEC) and enterohemorrhagic E. coli (EHEC). Phylogenetic analyses of 1,144 core E. coli genes indicate that the HUS-causing O104:H4 strains and the previously published sequence of the EAEC strain 55989 show a close relationship but are only distantly related to common EHEC serotypes. Though closely related, the outbreak strain differs from the 2001 strain in plasmid content and fimbrial genes. We propose a model in which EAEC 55989 and EHEC O104:H4 strains evolved from a common EHEC O104:H4 progenitor, and suggest that by stepwise gain and loss of chromosomal and plasmid-encoded virulence factors, a highly pathogenic hybrid of EAEC and EHEC emerged as the current outbreak clone. In conclusion, rapid next-generation technologies facilitated prospective whole genome characterization in the early stages of an outbreak. An ongoing outbreak of exceptionally virulent Shiga toxin (Stx)-producing Escherichia coli O104:H4 centered in Germany, has caused over 830 cases of hemolytic uremic syndrome (HUS) and 46 deaths since May 2011. Serotype O104:H4, which has not been detected in animals, has rarely been associated with HUS in the past. To prospectively elucidate the unique characteristics of this strain in the early stages of this outbreak, we applied whole genome sequencing on the Life Technologies Ion Torrent PGM™ sequencer and Optical Mapping to characterize one outbreak isolate (LB226692) and a historic O104:H4 HUS isolate from 2001 (01-09591). Reference guided draft assemblies of both strains were completed with the newly introduced PGM™ within 62 hours. The HUS-associated strains both carried genes typically found in two types of pathogenic E. coli , enteroaggregative E. coli (EAEC) and enterohemorrhagic E. coli (EHEC). Phylogenetic analyses of 1,144 core E. coli genes indicate that the HUS-causing O104:H4 strains and the previously published sequence of the EAEC strain 55989 show a close relationship but are only distantly related to common EHEC serotypes. Though closely related, the outbreak strain differs from the 2001 strain in plasmid content and fimbrial genes. We propose a model in which EAEC 55989 and EHEC O104:H4 strains evolved from a common EHEC O104:H4 progenitor, and suggest that by stepwise gain and loss of chromosomal and plasmid-encoded virulence factors, a highly pathogenic hybrid of EAEC and EHEC emerged as the current outbreak clone. In conclusion, rapid next-generation technologies facilitated prospective whole genome characterization in the early stages of an outbreak. An ongoing outbreak of exceptionally virulent Shiga toxin (Stx)-producing Escherichia coli O104:H4 centered in Germany, has caused over 830 cases of hemolytic uremic syndrome (HUS) and 46 deaths since May 2011. Serotype O104:H4, which has not been detected in animals, has rarely been associated with HUS in the past. To prospectively elucidate the unique characteristics of this strain in the early stages of this outbreak, we applied whole genome sequencing on the Life Technologies Ion Torrent PGM™ sequencer and Optical Mapping to characterize one outbreak isolate (LB226692) and a historic O104:H4 HUS isolate from 2001 (01-09591). Reference guided draft assemblies of both strains were completed with the newly introduced PGM™ within 62 hours. The HUS-associated strains both carried genes typically found in two types of pathogenic E. coli, enteroaggregative E. coli (EAEC) and enterohemorrhagic E. coli (EHEC). Phylogenetic analyses of 1,144 core E. coli genes indicate that the HUS-causing O104:H4 strains and the previously published sequence of the EAEC strain 55989 show a close relationship but are only distantly related to common EHEC serotypes. Though closely related, the outbreak strain differs from the 2001 strain in plasmid content and fimbrial genes. We propose a model in which EAEC 55989 and EHEC O104:H4 strains evolved from a common EHEC O104:H4 progenitor, and suggest that by stepwise gain and loss of chromosomal and plasmid-encoded virulence factors, a highly pathogenic hybrid of EAEC and EHEC emerged as the current outbreak clone. In conclusion, rapid next-generation technologies facilitated prospective whole genome characterization in the early stages of an outbreak.An ongoing outbreak of exceptionally virulent Shiga toxin (Stx)-producing Escherichia coli O104:H4 centered in Germany, has caused over 830 cases of hemolytic uremic syndrome (HUS) and 46 deaths since May 2011. Serotype O104:H4, which has not been detected in animals, has rarely been associated with HUS in the past. To prospectively elucidate the unique characteristics of this strain in the early stages of this outbreak, we applied whole genome sequencing on the Life Technologies Ion Torrent PGM™ sequencer and Optical Mapping to characterize one outbreak isolate (LB226692) and a historic O104:H4 HUS isolate from 2001 (01-09591). Reference guided draft assemblies of both strains were completed with the newly introduced PGM™ within 62 hours. The HUS-associated strains both carried genes typically found in two types of pathogenic E. coli, enteroaggregative E. coli (EAEC) and enterohemorrhagic E. coli (EHEC). Phylogenetic analyses of 1,144 core E. coli genes indicate that the HUS-causing O104:H4 strains and the previously published sequence of the EAEC strain 55989 show a close relationship but are only distantly related to common EHEC serotypes. Though closely related, the outbreak strain differs from the 2001 strain in plasmid content and fimbrial genes. We propose a model in which EAEC 55989 and EHEC O104:H4 strains evolved from a common EHEC O104:H4 progenitor, and suggest that by stepwise gain and loss of chromosomal and plasmid-encoded virulence factors, a highly pathogenic hybrid of EAEC and EHEC emerged as the current outbreak clone. In conclusion, rapid next-generation technologies facilitated prospective whole genome characterization in the early stages of an outbreak. |
| Audience | Academic |
| Author | Szczepanowski, Rafael Bielaszewska, Martina Moore, Richard L. Brzoska, Pius M. Cummings, Craig A. Guenther, Simone Rothberg, Jonathan M. Rico, Alain Prior, Karola Leopold, Shana R. Harmsen, Dag McLaughlin, Stephen F. Zentz, Emily B. Henkhaus, John K. Leopold, Benjamin Karch, Helge Zhang, Wenlan Ji, Yongmei Prager, Rita Mellmann, Alexander |
| AuthorAffiliation | 6 Robert Koch Institute, Wernigerode Branch, Wernigerode, Germany 7 Ion Torrent by Life Technologies, Guilford, Connecticut, United States of America University of Hyderabad, India 1 Institute of Hygiene, University Münster, Münster, Germany 2 Department of Periodontology, University Münster, Münster, Germany 3 Life Technologies, Foster City, California, United States of America 4 OpGen, Gaithersburg, Maryland, United States of America 5 Life Technologies, Darmstadt, Germany |
| AuthorAffiliation_xml | – name: 6 Robert Koch Institute, Wernigerode Branch, Wernigerode, Germany – name: 2 Department of Periodontology, University Münster, Münster, Germany – name: 5 Life Technologies, Darmstadt, Germany – name: 3 Life Technologies, Foster City, California, United States of America – name: 7 Ion Torrent by Life Technologies, Guilford, Connecticut, United States of America – name: 1 Institute of Hygiene, University Münster, Münster, Germany – name: 4 OpGen, Gaithersburg, Maryland, United States of America – name: University of Hyderabad, India |
| Author_xml | – sequence: 1 givenname: Alexander surname: Mellmann fullname: Mellmann, Alexander – sequence: 2 givenname: Dag surname: Harmsen fullname: Harmsen, Dag – sequence: 3 givenname: Craig A. surname: Cummings fullname: Cummings, Craig A. – sequence: 4 givenname: Emily B. surname: Zentz fullname: Zentz, Emily B. – sequence: 5 givenname: Shana R. surname: Leopold fullname: Leopold, Shana R. – sequence: 6 givenname: Alain surname: Rico fullname: Rico, Alain – sequence: 7 givenname: Karola surname: Prior fullname: Prior, Karola – sequence: 8 givenname: Rafael surname: Szczepanowski fullname: Szczepanowski, Rafael – sequence: 9 givenname: Yongmei surname: Ji fullname: Ji, Yongmei – sequence: 10 givenname: Wenlan surname: Zhang fullname: Zhang, Wenlan – sequence: 11 givenname: Stephen F. surname: McLaughlin fullname: McLaughlin, Stephen F. – sequence: 12 givenname: John K. surname: Henkhaus fullname: Henkhaus, John K. – sequence: 13 givenname: Benjamin surname: Leopold fullname: Leopold, Benjamin – sequence: 14 givenname: Martina surname: Bielaszewska fullname: Bielaszewska, Martina – sequence: 15 givenname: Rita surname: Prager fullname: Prager, Rita – sequence: 16 givenname: Pius M. surname: Brzoska fullname: Brzoska, Pius M. – sequence: 17 givenname: Richard L. surname: Moore fullname: Moore, Richard L. – sequence: 18 givenname: Simone surname: Guenther fullname: Guenther, Simone – sequence: 19 givenname: Jonathan M. surname: Rothberg fullname: Rothberg, Jonathan M. – sequence: 20 givenname: Helge surname: Karch fullname: Karch, Helge |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21799941$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2011 Public Library of Science 2011 Mellmann et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Mellmann et al. 2011 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: AM DH CAC SG JMR HK. Performed the Ion Torrent sequencing: DH KP RS WZ AR SG. Performed Optical Mapping: EBZ JKH RLM. Performed genome assembly: CAC YJ SFM PMB. Performed phylogenetic analysis: AM DH SL BL. Performed and analyzed plasmid profiling: MB RP. First draft of manuscript: AM DH CAC. Approved the final version of the manuscript: AM DH CAC EBZ SRL AR KP RS YJ WZ SFM JKH BL MB RP PMB RLM SG JMR HK. |
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| Snippet | An ongoing outbreak of exceptionally virulent Shiga toxin (Stx)-producing Escherichia coli O104:H4 centered in Germany, has caused over 830 cases of hemolytic... An ongoing outbreak of exceptionally virulent Shiga toxin (Stx)-producing Escherichia coli O104:H4 centered in Germany, has caused over 830 cases of hemolytic... |
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| SubjectTerms | Adult Antigens Automation Bacteria Bioinformatics Biology Deoxyribonucleic acid Diarrhea Disease Outbreaks DNA DNA sequencing E coli Enterohemorrhagic Escherichia coli - genetics Enterohemorrhagic Escherichia coli - pathogenicity Escherichia coli Escherichia coli Infections - epidemiology Evolution, Molecular Gene mapping Gene sequencing Genes Genomes Genomics Genomics - methods Germany - epidemiology Hemolytic uremic syndrome Humans Hygiene Laboratories Medicine Outbreaks Phylogeny Plasmids Prospective Studies Sequence Analysis, DNA - methods Serotypes Shiga toxin Time Factors Toxins Virulence Virulence factors |
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| Title | Prospective Genomic Characterization of the German Enterohemorrhagic Escherichia coli O104:H4 Outbreak by Rapid Next Generation Sequencing Technology |
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