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      Whole-Genome-Based Public Health Surveillance of Less Common Shiga Toxin-Producing Escherichia coli Serovars and Untypeable Strains Identifies Four Novel O Genotypes

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          Abstract

          Shiga toxin-producing Escherichia coli (STEC) and the STEC subgroup enterohemorrhagic E. coli cause intestinal infections with symptoms ranging from watery diarrhea to hemolytic-uremic syndrome (HUS). A key tool for the epidemiological differentiation of STEC is serotyping. The serotype in combination with the main virulence determinants gives important insight into the virulence potential of a strain.

          ABSTRACT

          Shiga toxin-producing Escherichia coli (STEC) and the STEC subgroup enterohemorrhagic E. coli cause intestinal infections with symptoms ranging from watery diarrhea to hemolytic-uremic syndrome (HUS). A key tool for the epidemiological differentiation of STEC is serotyping. The serotype in combination with the main virulence determinants gives important insight into the virulence potential of a strain. However, a large fraction of STEC strains found in human disease, including strains causing HUS, belongs to less frequently detected STEC serovars or their O/H antigens are unknown or even untypeable. Recent implementation of whole-genome sequence (WGS) analysis, in principle, allows the deduction of serovar and virulence gene information. Therefore, here we compared classical serovar and PCR-based virulence marker detection with WGS-based methods for 232 STEC strains, focusing on less frequently detected STEC serovars and nontypeable strains. We found that the results of WGS-based extraction showed a very high degree of overlap with those of the more classical methods. Specifically, the rate of concordance was 97% for O antigens (OAGs) and 99% for H antigens (HAGs) of typeable strains and >99% for stx 1, stx 2, or eaeA for all strains. Ninety-eight percent of nontypeable OAGs and 100% of nontypeable HAGs were defined by WGS analysis. In addition, the novel methods enabled a more complete analysis of strains causing severe clinical symptoms and the description of four novel STEC OAG loci. In conclusion, WGS is a promising tool for gaining serovar and virulence gene information, especially from a public health perspective.

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          Most cited references33

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          Analysis of Collection of Hemolytic Uremic Syndrome–associated Enterohemorrhagic Escherichia coli

          Multilocus sequence typing of 169 non-O157 enterohemorrhagic Escherichia coli (EHEC) isolated from patients with hemolytic uremic syndrome (HUS) demonstrated 29 different sequence types (STs); 78.1% of these strains clustered in 5 STs. From all STs and serotypes identified, we established a reference panel of EHEC associated with HUS (HUSEC collection).
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            The Type 1 secretion pathway - the hemolysin system and beyond.

            Type 1 secretion systems (T1SS) are wide-spread among Gram-negative bacteria. An important example is the secretion of the hemolytic toxin HlyA from uropathogenic strains. Secretion is achieved in a single step directly from the cytosol to the extracellular space. The translocation machinery is composed of three indispensable membrane proteins, two in the inner membrane, and the third in the outer membrane. The inner membrane proteins belong to the ABC transporter and membrane fusion protein families (MFPs), respectively, while the outer membrane component is a porin-like protein. Assembly of the three proteins is triggered by accumulation of the transport substrate (HlyA) in the cytoplasm, to form a continuous channel from the inner membrane, bridging the periplasm and finally to the exterior. Interestingly, the majority of substrates of T1SS contain all the information necessary for targeting the polypeptide to the translocation channel - a specific sequence at the extreme C-terminus. Here, we summarize our current knowledge of regulation, channel assembly, translocation of substrates, and in the case of the HlyA toxin, its interaction with host membranes. We try to provide a complete picture of structure function of the components of the translocation channel and their interaction with the substrate. Although we will place the emphasis on the paradigm of Type 1 secretion systems, the hemolysin A secretion machinery from E. coli, we also cover as completely as possible current knowledge of other examples of these fascinating translocation systems. This article is part of a Special Issue entitled: Protein trafficking and secretion in bacteria. Guest Editors: Anastassios Economou and Ross Dalbey. © 2013 Elsevier B.V. All rights reserved.
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              A complete view of the genetic diversity of the Escherichia coli O-antigen biosynthesis gene cluster

              The O antigen constitutes the outermost part of the lipopolysaccharide layer in Gram-negative bacteria. The chemical composition and structure of the O antigen show high levels of variation even within a single species revealing itself as serological diversity. Here, we present a complete sequence set for the O-antigen biosynthesis gene clusters (O-AGCs) from all 184 recognized Escherichia coli O serogroups. By comparing these sequences, we identified 161 well-defined O-AGCs. Based on the wzx/wzy or wzm/wzt gene sequences, in addition to 145 singletons, 37 serogroups were placed into 16 groups. Furthermore, phylogenetic analysis of all the E. coli O-serogroup reference strains revealed that the nearly one-quarter of the 184 serogroups were found in the ST10 lineage, which may have a unique genetic background allowing a more successful exchange of O-AGCs. Our data provide a complete view of the genetic diversity of O-AGCs in E. coli showing a stronger association between host phylogenetic lineage and O-serogroup diversification than previously recognized. These data will be a valuable basis for developing a systematic molecular O-typing scheme that will allow traditional typing approaches to be linked to genomic exploration of E. coli diversity.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                J Clin Microbiol
                J. Clin. Microbiol
                jcm
                jcm
                JCM
                Journal of Clinical Microbiology
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                0095-1137
                1098-660X
                31 July 2019
                24 September 2019
                October 2019
                24 September 2019
                : 57
                : 10
                : e00768-19
                Affiliations
                [a ]Division of Enteropathogenic Bacteria and Legionella, National Reference Centre for Salmonella and Other Enteric Bacterial Pathogens, Robert Koch Institute, Wernigerode, Germany
                [b ]Department of Infectiology, Bavarian Health and Food Safety Authority, Oberschleissheim, Germany
                Medical College of Wisconsin
                Author notes
                Address correspondence to Antje Flieger, fliegera@ 123456rki.de .

                Citation Lang C, Hiller M, Konrad R, Fruth A, Flieger A. 2019. Whole-genome-based public health surveillance of less common Shiga toxin-producing Escherichia coli serovars and untypeable strains identifies four novel O genotypes. J Clin Microbiol 57:e00768-19. https://doi.org/10.1128/JCM.00768-19.

                Article
                00768-19
                10.1128/JCM.00768-19
                6760944
                31366691
                0e1c146a-d8c9-42ab-82c5-8267f7365c7f
                Copyright © 2019 Lang et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 14 May 2019
                : 12 June 2019
                : 22 July 2019
                Page count
                supplementary-material: 1, Figures: 5, Tables: 2, Equations: 0, References: 46, Pages: 12, Words: 7555
                Categories
                Epidemiology
                Custom metadata
                October 2019

                Microbiology & Virology
                genoserotyping,public health surveillance,stec,whole-genome sequencing
                Microbiology & Virology
                genoserotyping, public health surveillance, stec, whole-genome sequencing

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