O-Antigen Diversification Masks Identification of Highly Pathogenic Shiga Toxin-Producing Escherichia coli O104:H4-Like Strains
ABSTRACT Shiga toxin-producing Escherichia coli (STEC) can give rise to a range of clinical outcomes from diarrhea to the life-threatening systemic condition hemolytic-uremic syndrome (HUS). Although STEC O157:H7 is the serotype most frequently associated with HUS, a major outbreak of HUS occurred i...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00987-23 |
| _version_ | 1797803399448625152 |
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| author | Christina Lang Angelika Fruth Ian W. Campbell Claire Jenkins Peyton Smith Nancy Strockbine François-Xavier Weill Ulrich Nübel Yonatan H. Grad Matthew K. Waldor Antje Flieger |
| author_facet | Christina Lang Angelika Fruth Ian W. Campbell Claire Jenkins Peyton Smith Nancy Strockbine François-Xavier Weill Ulrich Nübel Yonatan H. Grad Matthew K. Waldor Antje Flieger |
| author_sort | Christina Lang |
| collection | DOAJ |
| description | ABSTRACT Shiga toxin-producing Escherichia coli (STEC) can give rise to a range of clinical outcomes from diarrhea to the life-threatening systemic condition hemolytic-uremic syndrome (HUS). Although STEC O157:H7 is the serotype most frequently associated with HUS, a major outbreak of HUS occurred in 2011 in Germany and was caused by a rare serotype, STEC O104:H4. Prior to 2011 and since the outbreak, STEC O104:H4 strains have only rarely been associated with human infections. From 2012 to 2020, intensified STEC surveillance was performed in Germany where the subtyping of ~8,000 clinical isolates by molecular methods, including whole-genome sequencing, was carried out. A rare STEC serotype, O181:H4, associated with HUS was identified, and like the STEC O104:H4 outbreak strain, this strain belongs to sequence type 678 (ST678). Genomic and virulence comparisons revealed that the two strains are phylogenetically related and differ principally in the gene cluster encoding their respective lipopolysaccharide O-antigens but exhibit similar virulence phenotypes. In addition, five other serotypes belonging to ST678 from human clinical infection, such as OX13:H4, O127:H4, OgN-RKI9:H4, O131:H4, and O69:H4, were identified from diverse locations worldwide. IMPORTANCE Our data suggest that the high-virulence ensemble of the STEC O104:H4 outbreak strain remains a global threat because genomically similar strains cause disease worldwide but that the horizontal acquisition of O-antigen gene clusters has diversified the O-antigens of strains belonging to ST678. Thus, the identification of these highly pathogenic strains is masked by diverse and rare O-antigens, thereby confounding the interpretation of their potential risk. |
| first_indexed | 2024-03-13T05:21:26Z |
| format | Article |
| id | doaj.art-7e0d62069fa240dda480fcedf8769d55 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-13T05:21:26Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-7e0d62069fa240dda480fcedf8769d552023-06-15T13:18:32ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.00987-23O-Antigen Diversification Masks Identification of Highly Pathogenic Shiga Toxin-Producing Escherichia coli O104:H4-Like StrainsChristina Lang0Angelika Fruth1Ian W. Campbell2Claire Jenkins3Peyton Smith4Nancy Strockbine5François-Xavier Weill6Ulrich Nübel7Yonatan H. Grad8Matthew K. Waldor9Antje Flieger10Division of Enteropathogenic Bacteria and Legionella, National Reference Centre for Salmonella and Other Enteric Bacterial Pathogens, Robert Koch Institut, Wernigerode, GermanyDivision of Enteropathogenic Bacteria and Legionella, National Reference Centre for Salmonella and Other Enteric Bacterial Pathogens, Robert Koch Institut, Wernigerode, GermanyDepartment of Microbiology, Division of Infectious Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USAGastro and Food Safety (One Health) Division, Health Security Agency, London, United KingdomDivision of Foodborne, Waterborne and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USADivision of Foodborne, Waterborne and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USAInstitut Pasteur, Université Paris Cité, Unité des Bactéries Pathogènes Entériques, Paris, FranceLeibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, GermanyDepartment of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, USADepartment of Microbiology, Division of Infectious Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USADivision of Enteropathogenic Bacteria and Legionella, National Reference Centre for Salmonella and Other Enteric Bacterial Pathogens, Robert Koch Institut, Wernigerode, GermanyABSTRACT Shiga toxin-producing Escherichia coli (STEC) can give rise to a range of clinical outcomes from diarrhea to the life-threatening systemic condition hemolytic-uremic syndrome (HUS). Although STEC O157:H7 is the serotype most frequently associated with HUS, a major outbreak of HUS occurred in 2011 in Germany and was caused by a rare serotype, STEC O104:H4. Prior to 2011 and since the outbreak, STEC O104:H4 strains have only rarely been associated with human infections. From 2012 to 2020, intensified STEC surveillance was performed in Germany where the subtyping of ~8,000 clinical isolates by molecular methods, including whole-genome sequencing, was carried out. A rare STEC serotype, O181:H4, associated with HUS was identified, and like the STEC O104:H4 outbreak strain, this strain belongs to sequence type 678 (ST678). Genomic and virulence comparisons revealed that the two strains are phylogenetically related and differ principally in the gene cluster encoding their respective lipopolysaccharide O-antigens but exhibit similar virulence phenotypes. In addition, five other serotypes belonging to ST678 from human clinical infection, such as OX13:H4, O127:H4, OgN-RKI9:H4, O131:H4, and O69:H4, were identified from diverse locations worldwide. IMPORTANCE Our data suggest that the high-virulence ensemble of the STEC O104:H4 outbreak strain remains a global threat because genomically similar strains cause disease worldwide but that the horizontal acquisition of O-antigen gene clusters has diversified the O-antigens of strains belonging to ST678. Thus, the identification of these highly pathogenic strains is masked by diverse and rare O-antigens, thereby confounding the interpretation of their potential risk.https://journals.asm.org/doi/10.1128/spectrum.00987-23O-antigen diversificationO104:H4Shiga toxin-producing E. coliphylogenyrisk profiling |
| spellingShingle | Christina Lang Angelika Fruth Ian W. Campbell Claire Jenkins Peyton Smith Nancy Strockbine François-Xavier Weill Ulrich Nübel Yonatan H. Grad Matthew K. Waldor Antje Flieger O-Antigen Diversification Masks Identification of Highly Pathogenic Shiga Toxin-Producing Escherichia coli O104:H4-Like Strains Microbiology Spectrum O-antigen diversification O104:H4 Shiga toxin-producing E. coli phylogeny risk profiling |
| title | O-Antigen Diversification Masks Identification of Highly Pathogenic Shiga Toxin-Producing Escherichia coli O104:H4-Like Strains |
| title_full | O-Antigen Diversification Masks Identification of Highly Pathogenic Shiga Toxin-Producing Escherichia coli O104:H4-Like Strains |
| title_fullStr | O-Antigen Diversification Masks Identification of Highly Pathogenic Shiga Toxin-Producing Escherichia coli O104:H4-Like Strains |
| title_full_unstemmed | O-Antigen Diversification Masks Identification of Highly Pathogenic Shiga Toxin-Producing Escherichia coli O104:H4-Like Strains |
| title_short | O-Antigen Diversification Masks Identification of Highly Pathogenic Shiga Toxin-Producing Escherichia coli O104:H4-Like Strains |
| title_sort | o antigen diversification masks identification of highly pathogenic shiga toxin producing escherichia coli o104 h4 like strains |
| topic | O-antigen diversification O104:H4 Shiga toxin-producing E. coli phylogeny risk profiling |
| url | https://journals.asm.org/doi/10.1128/spectrum.00987-23 |
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