Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-11T07:03:02.190Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular serogrouping of Escherichia coli

Published online by Cambridge University Press:  22 February 2018

Chitrita DebRoy ,
Pina M. Fratamico  and
Elisabeth Roberts
Chitrita DebRoy*
Affiliation:
Department of Veterinary and Biomedical Sciences, E. coli Reference Center, The Pennsylvania State University, University Park, PA, USA
Pina M. Fratamico
Affiliation:
U.S. Department of Agriculture, Eastern Regional Research Center, Agricultural Research Service, Wyndmoor, PA, USA
Elisabeth Roberts
Affiliation:
Department of Veterinary and Biomedical Sciences, E. coli Reference Center, The Pennsylvania State University, University Park, PA, USA
*
*Corresponding author. E-mail: rcd3@psu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

O-antigens present on the surface of Escherichia coli provide antigenic specificity for the strain and are the main components for O-serogroup designation. Serotyping using O-group-specific antisera for the identification of E. coli O-serogroups has been traditionally the gold-standard for distinguishing E. coli strains. Knowledge of the O-group is important for determining pathogenic lineage, classifying E. coli for epidemiological studies, for determining virulence, and for tracing outbreaks of diseases and sources of infection. However, serotyping has limitations, as the antisera generated against each specific O-group may cross-react, many strains are non-typeable, and others can autoagglutinate or be rough (lacking an O-antigen). Currently, the nucleotide sequences are available for most of the 187 designated E. coli O-groups. Public health and other laboratories are considering whole genome sequencing to develop genotypic methods to determine O-groups. These procedures require instrumentation and analysis that may not be accessible and may be cost-prohibitive at this time. In this review, we have identified unique gene sequences within the O-antigen gene clusters and have targeted these genes for identification of O-groups using the polymerase chain reaction. This information can be used to distinguish O-groups by developing other platforms for E. coli diagnostics in the future.

Keywords

serotypinggenotypingPCRsequencingO-antigen gene cluster
Type
Review Article
Information
Animal Health Research Reviews , Volume 19 , Issue 1 , June 2018 , pp. 1 - 16
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbadi, SH and Strockbine, NA (2007). Identification of Escherichia coli flagellar types by restriction of the amplified fliC gene. Egyptian Journal of Medical Microbiology 16: 225–233.Google Scholar
Achtman, M and Pluschke, G (1986). Clonal analysis of descent and virulence among selected Escherichia coli. Annual Review of Microbiology 40: 185–210.Google Scholar
Akira, S, Uematsu, S and Takeuchi, O (2006). Pathogen recognition and innate immunity. Cell 124: 783–801.Google Scholar
Bastin, DA, Stevenson, G, Brown, AH and Reeves, PR (1993). Repeat unit polysaccharides of bacteria: a model for polymerization resembling that of ribosomes and fatty acid synthetase, with a novel mechanism for determining chain length. Molecular Microbiology 7: 725–734.Google Scholar
Batchelor, RA, Alifano, P, Biffali, E, Hull, SI and Hull, RA (1992). Nucleotide sequences of the genes regulating O-polysaccharide antigen chain length (rol) from Escherichia coli and Salmonella typhimurium: protein homology and functional complementation. Journal of Bacteriology 174: 5228–5236.Google Scholar
Beutin, L, Strauch, E, Zimmermann, S, Kaulfuss, S, Schaudinn, C, Männel, A and Gelderblom, HR (2005a). Genetical and functional investigation of fliC genes encoding flagellar serotype H4 in wildtype strains of Escherichia coli and in a laboratory E. coli K-12 strain expressing flagellar antigen type H48. BMC Microbiology 5: 4.Google Scholar
Beutin, L, Kong, Q, Feng, L, Wang, Q, Krause, G, Leomil, L, Jin, Q and Wang, L (2005b). Development of PCR assays targeting the genes involved in synthesis and assembly of the new Escherichia coli O174 and O177 O antigens. Journal of Clinical Microbiology 43: 5143–5149.Google Scholar
Bos, MP, Robert, V and Tommassen, J (2007). Biogenesis of Gram-negative bacterial outer membrane. Annual Review of Microbiology 61: 191–214.Google Scholar
Botkin, DJ, Galli, L, Sankarapani, V, Soler, M, Rivas, M and Torres, AG (2012). Development of a multiplex PR assay for detection of Shiga toxin-producing Escherichia coli, enterohemorrhagic E. coli, and enteropathogenic E. coli strains. Frontiers in Cellular and Infection Microbiology 2: 8.Google Scholar
Bronner, D, Clarke, BR and Whitfield, C (1994). Identification of an ATP-binding cassette transport system required for translocation of lipopolysachharide O-antigen side-chains across the cytoplasmic membrane of Klebsiella pneumonia serotype O1. Molecular Microbiology 14: 505–519.Google Scholar
Bugarel, M, Beutin, L, Martin, A, Gill, A and Fach, P (2010). Micro-array for the identification of Shiga toxin-producing Escherichia coli (STEC) seropathotypes associated with hemorrhagic colitis and hemolytic uremic syndrome in humans. International Journal of Food Microbiology 142: 318–329.Google Scholar
Carvallo, F, DebRoy, C, Baeza, E, Hinckley, L and Gilbert, K (2010). Extraintestinal pathogenic Escherichia coli induced necrotizing pneumonia in a white tiger cub. Journal of Veterinary Diagnostic Investigation 22: 136–140.Google Scholar
Chafchaouni-Moussaoui, I, Novikov, A, Bhrada, F, Perry, MB, Filali-Maltouf, A and Caroff, M (2011). A new rapid and micro-scale hydrolysis, using triethylamine citrate, for lipopolysaccharide characterization by mass spectrometry. Rapid Communication in Mass Spectrometry 14: 2043–2048.Google Scholar
Cheng, J, Wang, Q, Wang, W, Wang, Y, Wang, L and Feng, L (2006). Characterization of E. Coli O24 and O56 O antigen gene clusters reveals a complex evolutionary history of the O24 gene cluster. Current Microbiology 53: 470–476.Google Scholar
Cheng, J, Liu, B, Bastin, DA, Han, W, Wang, L and Feng, L (2007). Genetic characterization of the Escherichia coli O66 antigen and functional identification of its wzy gene. Journal of Microbiology 45: 69–74.Google Scholar
Coimbra, RS, Grimont, F, Lenormand, P, Burguière, P, Beutin, L and Grimont, PAD (2000). Identification of Escherichia coli O-serogroups by restriction of the amplified O-antigen gene cluster (rfp-RFLP). Research in Microbiology 151: 639–654.Google Scholar
Daniels, C, Vindurampulle, C and Morona, R (1998). Overexpression and topology of Shigella flexneri O antigen polymerase (Rfc/Wzy). Molecular Microbiology 28: 1211–1222.Google Scholar
DebRoy, C, Roberts, E, Kundrat, J, Davis, MA, Briggs, CE and Fratamico, PM (2004). Detection of Escherichia coli serogroups O26 and O113 by PCR amplification of wzx and wzy genes. Applied and Environmental Microbiology 70: 1830–1832.Google Scholar
DebRoy, C, Fratamico, PM, Roberts, E, Davis, MA and Liu, Y (2005). Development of PCR assays targeting genes in O-antigen gene clusters for detection and identification of Escherichia coli O45 and O55 serogroups. Applied and Environmental Microbiology 71: 4919–4924.Google Scholar
DebRoy, C, Roberts, E, Jayarao, BM and Brooks, JW (2008). Bronchopneumonia associated with extraintestinal pathogenic Escherichia coli in a horse. Journal of Veterinary Diagnostic Investigations 20: 661–664.Google Scholar
DebRoy, C, Roberts, E, Davis, MA and Bumbaugh, AC (2010). Detection of non-serotypable Shiga toxin-producing Escherichia coli strains derived from pigs by multiplex PCR assay. Foodborne Pathogens and Disease 7: 1407–1414.Google Scholar
DebRoy, C, Roberts, E and Fratamico, PM (2011a). Detection of O antigens in Escherichia coli. Animal Health Research Review 12: 169–185.Google Scholar
DebRoy, C, Roberts, E, Valadez, AM, Dudley, EG and Cutter, CN (2011b). Detection of Shiga toxin producing Escherichia coli O26, O45, O103, O111, O113, O121, O145, and O157 serogroups by multiplex PCR of the wzx gene of the O-antigen gene cluster. Foodborne Pathogens and Disease 8: 651–652.Google Scholar
DebRoy, C, Fratamico, PM, Yan, X, Baranzoni, GM, Liu, Y, Needleman, DS, Tebbs, R, O'Connell, CD, Allred, A, Swimley, M, Mwangi, M, Kapur, V, Raygoza Garay, JA, Roberts, EL and Katani, R (2016). Comparison of O-antigen gene clusters of all O-serogroups of Escherichia coli and proposal for adopting a new nomenclature for O-typing. PLoS ONE 11: e0147434. doi: 10.1371/journal.pone.0147434.Google Scholar
Delannoy, S, Beutin, L and Fach, P (2013). Discrimination of enterohemorrhagic Escherichia coli (EHEC) from non-EHEC strains based on detection of various combinations of type III effector genes. Journal of Clinical Microbiology 51: 3257–3262.Google Scholar
Dickinson, CE, Gould, DH, Davidson, AH, Avery, PR, Legare, ME, Hyatt, DR and DebRoy, C (2008). Hemolytic-uremic syndrome in a postpartum mare concurrent with encephalopathy in the neonatal foal. Journal of Veterinary Diagnostic Investigation 20: 239–242.Google Scholar
Doumith, M, Day, MJ, Hope, R, Wain, J and Woodford, N (2012). Improved multiplex PCR strategy for rapid assignment of the four major Escherichia coli phylogenetic groups. Journal of Clinical Microbiology 50: 3108–3110.Google Scholar
Ewing, WH (1986). The genus shigella. In: Edwards, PR and Ewing, WH (eds) Edwards and Ewing's Identification of Enterobacteriaceae, 4th edn. New York: Elsevier Science Publishing Co., Inc, pp. 135–172.Google Scholar
Ewing, WH and Tatum, HW (1956). US Communicable Disease Center. Studies on the serology of the Escherichia coli group. [Available online at http://www.worldcat.org/title/studies-on-the-serology-of-the-escherichia-coli-group/oclc/654668490].Google Scholar
Feng, L, Wang, W, Tao, J, Guo, H, Krause, G, Beutin, L and Wang, L (2004). Identification of Escherichia coli O114 O-antigen gene cluster and development of an O114 serogroup-specific PCR assay. Journal of Clinical Microbiology 42: 3799–3804.Google Scholar
Feng, L, Han, W, Wang, Q, Bastin, DA and Wang, L (2005). Characterization of Escherichia coli O86 O-antigen gene cluster and identification of O86-specific genes. Veterinary Microbiology 106: 241–248.Google Scholar
Fratamico, PM and DebRoy, C (2010). Detection of Escherichia coli O157:H7 in food using real-time multiplex PCR assays targeting the stx1, stx2, wzyO157, and the fliCh7 or eae genes. Food Analytical Methods 3: 330–337.Google Scholar
Fratamico, PM, Briggs, CE, Needle, D, Chen, CY and DebRoy, C (2003). Sequence of the Escherichia coli O121 O-antigen gene cluster and detection of enterohemorrhagic E. coli O121 by PCR amplification of the wzx and wzy genes. Journal of Clinical Microbiology 41: 3379–3383.Google Scholar
Fratamico, PM, DebRoy, C, Strobaugh, TP Jr and Chen, CY (2005). DNA sequence of the Escherichia coli O103 O antigen gene cluster and detection of enterohemorrhagic E. coli O103 by PCR amplification of the wzx and wzy genes. Canadian Journal of Microbiology 51: 515–522.Google Scholar
Fratamico, PM, DebRoy, C and Liu, Y (2009a). The DNA sequence of the Escherichia coli O22 O antigen gene cluster and detection of pathogenic strains belonging to E. coli serogroups O22 and O91 by multiplex PCR assays targeting virulence genes and genes in the respective O-antigen gene clusters. Food Analytical Methods 2: 169–179.Google Scholar
Fratamico, PM, DebRoy, C, Miyamoto, T and Liu, Y (2009b). Detection of entero-hemorrhagic Escherichia coli O145 in food by PCR targeting genes in the E. coli O145 O antigen gene cluster and the Shiga toxins 1 and 2 genes. Foodborne Pathogen and Disease 6: 605–611.Google Scholar
Fratamico, PM, Yan, X, Liu, Y, DebRoy, C, Byrne, B, Monaghan, A, Fanning, S and Bolton, D (2010). Escherichia coli serogroup O2 and O28ac O-antigen gene cluster sequences and detection of pathogenic E. coli O2 and O28ac by PCR. Canadian Journal of Microbiology 56: 308–316.Google Scholar
Fratamico, PM, Wasilenko, JL, Garman, B, DeMarco, DR, Varkey, S, Jensen, M, Rhoden, K and Tice, G (2014). Evaluation of a multiplex PCR real-time PCR method for detecting Shiga toxin-producing Escherichia coli in beef and comparison to the U.S. Department of Agriculture Food Safety and Inspection Service Microbiology Laboratory Guidebook Method. Journal of Food Protection 77: 180–188.Google Scholar
Grozdanov, L, Zahringer, U, Blum-Oehler, G, Brade, L, Henne, A, Knirel, YA, Schombel, U, Schulze, J, Sonnenborn, U, Gottschalk, G, Hacker, J, Rietschel, ET and Dobrindt, U (2002). A single nucleotide exchange in the wzy gene is responsible for the semirough O6 lipopolysaccharide phenotype and serum sensitivity of Escherichia coli strain Nissle 1917. Journal of Bacteriology 184: 5912–5925.Google Scholar
Guo, H, Feng, L, Tao, J, Zhang, C and Wang, L (2004). Identification of Escherichia coli O172 O-antigen gene cluster and development of a serogroup-specific PCR assay. Journal of Applied Microbiology 97: 181–190.Google Scholar
Han, W, Liu, B, Cao, B, Beutin, L, Kruger, U, Liu, H, Li, Y, Liu, Y, Feng, L and Wang, L (2007). DNA microarray-based identification of serogroups and virulence gene patterns of Escherichia coli isolates associated with porcine postweaning diarrhea and edema disease. Applied and Environmental Microbiology 73: 4082–4088.Google Scholar
Handt, LK, Stoffregen, DA, Prescott, JS, Pouch, WJ, Ngai, DTW, Anderson, CA, Gatto, NT, DebRoy, C, Fairbrother, JM, Motzel, SL and Klein, HJ (2003). Clinical and microbiologic characterization of hemorrhagic pneumonia due to extraintestinal pathogenic E. coli in four young dogs. Comparative Medicine 53: 663–670.Google Scholar
Hobbs, M and Reeves, PR (1994). The JUMPstart sequence: a 39 bp element common to several polysaccharide gene clusters. Molecular Microbiology 12: 855–856.Google Scholar
Hegde, NV, Jayarao, BM and DebRoy, C (2012). Rapid detection of the top six non-O157 Shiga toxin-producing Escherichia coli O groups in ground beef by flow cytometry. Journal of Clinical Microbiology 50: 2137–2139.Google Scholar
Hegde, NV, Praul, C, Gehring, A, Fratamico, PM and DebRoy, C (2013). Rapid identification of the six clinically relevant O serogroups of Shiga toxin-producing Escherichia coli by antibody microarray. Journal of Microbiological Methods 93: 273–276.Google Scholar
Hu, B, Perepelov, AV, Liu, B, Shevelev, SD, Guo, D, Senchenkova, SN, Shashkov, AS, Feng, L, Knirel, YA and Wang, L (2010). Structural and genetic evidence for the close relationship between Escherichia coli O71 and Salmonella enterica O28 O-antigens. FEMS Immunology and Medical Microbiology 59: 161–169.Google Scholar
Iguchi, A, Iyoda, S, Kikuchi, T, Ogura, Y, Katsura, K, Ohnishi, M, Hayashi, T and Thomson, NR (2015a). A complete view of the genetic diversity of the Escherichia coli O-antigen biosynthesis gene cluster. DNA Research 22: 101–107.Google Scholar
Iguchi, A, Iyoda, S, Seto, K, Morita-Ishihara, T, Sheutz, F, Ohnishi, M and Pathogenic, E. coli Working Group in Japan (2015b). Escherichia coli O-genotyping PCR: a comprehensive and practical platform for molecular O serogrouping. Journal of Clinical Microbiology 53: 2427–2432.Google Scholar
Iguchi, A, Iyoda, S, Seto, K, Nishii, H, Ohnishi, M, Mekata, H, Ogura, Y and Hayashi, T (2016). Six novel O genotypes from Shiga toxin-producing Escherichia coli. Frontiers in Microbiology 7: 765.Google Scholar
Ingle, DJ, Valcanis, M, Kuzevski, A, Tauschek, M, Inouye, M, Stinear, T, Levine, MM, Robins-Browne, RM and Holt, KE (2016). In silico serotyping of E. coli from short read data identifies limited novel O-loci but extensive diversity of O:H serotype combinations within and between pathogenic lineages. Microbial Genomics 2: e000064. doi: 10.1099/mgen.0.000064.Google Scholar
Ison, SA, Delannoy, S, Bugarel, M, Nagaraja, TG, Renter, DG, den Bakker, HC, Nightingale, KK, Fach, P, Loneragan, GH (2016). Targeted amplicon sequencing for single-nucleotide-polymorphism genotyping of attaching and effacing Escherichia coli O26:H11 cattle strains via a high-throughput library preparation technique. Applied and Environmental Microbiology 82: 640–649.Google Scholar
Joensen, KG, Scheutz, F, Lund, O, Hasman, H, Kaas, RS, Nielsen, EM and Aarestrup, FM (2014). Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. Journal of Clinical Microbiology 52: 1501–1510.Google Scholar
Joensen, KG, Tetzschner, AM, Iguchi, A, Aarestrup, FM and Scheutz, F (2015). Rapid and easy in silico serotyping of Escherichia coli using whole genome sequencing (WGS) data. Journal of Clinical Microbiology 53: 2410–2426.Google Scholar
Kaper, JB, Nataro, JP and Mobley, HL (2004). Pathogenic Escherichia coli. Nature Reviews Microbiology 2: 123–140.Google Scholar
Kaufmann, F (1943). Ueber neue tthermolabile Ko¨rperantigen der Colibakterien. Acta Pathologica et Microbiologica Scandinavica 20: 21–44.Google Scholar
Kaufmann, F (1944). Zur Serologie der Coli-Gruppe. Acta Pathologica et Microbiologica Scandinavica 21: 20–45.Google Scholar
Kaufmann, F (1947). The serology of E. coli group. Journal of Immunology 57: 71–100.Google Scholar
Keenleyside, WJ and Whitfield, C (1996). A novel pathway for O polysaccharide biosynthesis in Salmonella enterica serovar Borreze. Journal of Biological Chemistry 271: 28581–28592.Google Scholar
Knirel, YA, Qian, C, Shashkov, AS, Sizova, OV, Zdorovenko, EL, Naumenko, OI, Senchenkova, SN, Perepelov, AV and Liu, B (2016). Structural relationships between genetically closely related O-antigens of Escherichia coli and Shigella spp. Biochemistry (Moscow) 81: 600–608.Google Scholar
Kwong, JC, McCallum, N, Sintchenko, V and Howden, BP (2015). Whole genome sequencing in clinical and public health microbiology. Pathology 47: 199–210.Google Scholar
Lacher, DW, Gangiredla, J, Jackson, SA, Elkins, CA and Feng, PC (2014). Novel microarray design for molecular serotyping of Shiga toxin-producing Escherichia coli strains isolated from fresh produce. Applied and Environmental Microbiology 80: 4677–4682.Google Scholar
Li, D, Liu, B, Chen, M, Guo, D, Guo, X, Liu, F, Feng, L and Wang, L (2010). A multiplex PCR method to detect 14 Escherichia coli serogroups associated with urinary tract infections. Journal of Microbiological Methods 82: 71–77.Google Scholar
Li, Y, Perepelov, AV, Guo, D, Shevelev, SD, Senchenkova, SN, Shahskov, AS, Liu, B, Wang, L, Knirel, YA (2011). Structural and genetic relationships of two pairs of closely related O-antigens of Escherichia coli and Salmonella enterica: E. coli O11/S. Enterica O16 and E. coli O21/S. Enterica O38. FEMS Immunology and Medical Microbiology 61: 258–268.Google Scholar
Linton, KJ and Higgins, CF (1998). The Escherichia coli ATP binding cassette (ABC) proteins. Molecular Microbiology 28: 5–13.Google Scholar
Liu, B, Knirel, YA, Feng, L, Perepelov, AV, Senchenkova, SN, Wang, Q, Reeves, PR, Wang, L (2008a). Structure and genetics of Shigella O antigens. FEMS Microbiology Reviews 32: 627–653.Google Scholar
Liu, B, Wu, F, Li, D, Beutin, L, Chen, M, Cao, B and Wang, L (2010). Development of a serogroup-specific DNA microarray for identification of Escherichia coli strains associated with bovine septicemia and diarrhea. Veterinary Microbiology 142: 373–378.Google Scholar
Liu, Y and Fratamico, PM (2006). Escherichia coli O antigen typing using DNA microarrays. Molecular and Cellular Probes 20: 239–244.Google Scholar
Liu, Y, DebRoy, C and Fratamico, PM (2007). Sequencing and analysis of the Escherichia coli serogroup O117, O126, and O146 O-antigen gene clusters and development of PCR assays targeting serogroup O117-, O126-, and O146-specific DNA sequences. Molecular and Cellular Probes 21: 295–302.Google Scholar
Liu, Y, Fratamico, PM, DebRoy, C, Bumbaugh, AC and Allen, JW (2008b). DNA sequencing and identification of serogroup-specific genes in the Escherichia coli O118 O antigen gene cluster and demonstration of antigenic diversity but only minor variation in DNA sequence of the O antigen clusters of E. coli O118 and O151. Foodborne Pathogens and Disease 5: 449–457.Google Scholar
Liu, Y, Yan, X, DebRoy, C, Fratamico, PM, Needleman, DS, Li, R, Wang, W, Losada, L, Brinka, L, Radune, D, Toro, M, Hegde, N and Meng, J (2015). Escherichia coli O-antigen gene clusters of serogroups O62, O68, O131, O140, O142, and O163: DNA sequences and similarity between O62 and O68, and PCR-based serogrouping. Biosensors 5: 51–68.Google Scholar
MacLean, LL, Webb, AC and Perry, MB (2006). Structural elucidation of the O-antigenic polysaccharide from enterohemorrhagic (EHEC) Escherichia coli O48:H21. Carbohydrate Research 341: 2543–2549.Google Scholar
McGrath, BC and Osborn, MJ (1991). Localization of the terminal steps of O antigen synthesis in Salmonella typhimurium. Journal of Bacteriology 173: 649–654.Google Scholar
Moreno, ACR, Guth, BEC and Martinez, MB (2006). Can the fliC PCR-restriction fragment length polymorphism technique replace classic serotyping methods for characterizing the H antigen of enterotoxigenic Escherichia coli strains? Journal of Clinical Microbiology 44: 1453–1458.Google Scholar
Morona, R, Van Den Bosch, L and Manning, P (1995). Molecular, genetic, and topological characterization of O antigen chain regulation in Shigella flexneri. Journal of Bacteriology 177: 1059–1068.Google Scholar
Mulford, CA and Osborn, MJ (1983). An intermediate step in translocation of lipopolysaccharide to outer membrane of Salmonella typhimurium. Proceedings of the National Academy of Sciences USA 80: 1159–1163.Google Scholar
Norman, KN, Clawson, ML, Strockbine, NA, Mandrell, RE, Johnson, R, Ziebell, K, Zhao, S, Fratamico, PM, Stones, R, Allard, MW and Bono, JL (2015). Comparison of whole genome sequences from human and non-human Escherichia coli O26 strains. Frontiers in Cellular and Infection Microbiology 5: 21.Google Scholar
Ørskov, F and Ørskov, I (1984). Serotyping of Escherichia coli. Methods in Microbiology 14: 43–112.Google Scholar
Ørskov, I, Ørskov, F, Jann, B and Jann, K (1977). Serology, chemistry, and genetics of O and K antigens of Escherichia coli. Bacteriological Reviews 41: 667–710.Google Scholar
Patel, IR, Gangiredla, J, Lacher, DW, Mammel, MK, Jackson, SA, Lampel, KA and Elkins, CA (2016). FDA Escherichia coli identification (FDA-ECID) microarray: a pangenome molecular toolbox for serotyping, virulence profiling, molecular epidemiology, and phylogeny. Applied and Environmental Microbiology 82: 3384–3394.Google Scholar
Plainvert, C, Bidet, P, Peigne, C, Barbe, V, Médigue, C, Denamur, E, Bingen, E and Bonacorsi, S (2007). A new O-antigen gene cluster has a key role in the virulence of the Escherichia coli meningitis clone O45:K1:H7. Journal of Bacteriology 189: 8528–8536.Google Scholar
Poltorak, A, He, X, Smirnova, I, Liu, MY, Van Huffel, C, Du, X, Birdwell, D, Alejos, E, Silva, M, Galanos, C, Freudenberg, M, Ricciardi-Castagnoli, P, Layton, B and Beutler, B (1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085–2088.Google Scholar
Reeves, PR (1994). Biosynthesis and assembly of lipopolysaccharides. In Ghuysen, J-M and Hakenbeck, R (eds) New Comprehensive Biochemistry, Bacterial Cell Wall. Elsevier Science Publisher, Amsterdam, Chap. 13, pp. 281–317.Google Scholar
Reeves, PR and Wang, L (2002). Genomic organization of LPS-specific loci. Current Topics in Microbiological Immunology 264: 109–135.Google Scholar
Remis, RS, MacDonald, KL, Riley, LW, Puhr, ND, Wells, JG, Davis, BR, Blake, PA and Cohen, ML (1984). Sporadic cases of hemorrhagic colitis associated with Escherichia coli O157:H7. Annals of Internal Medicine 101: 624–626.Google Scholar
Ren, Y, Liu, B, Cheng, J, Liu, F, Feng, L and Wang, L (2008). Characterization of Escherichia coli O3 and O21 O antigen gene clusters and development of serogroup-specific PCR assays. Journal of Microbiological Methods 75: 329–334.Google Scholar
Riley, LW, Remis, RS, Helgerson, SD, McGee, HB, Wells, JG, Davis, BR, Hebert, RJ, Olcott, ES, Johnson, LM, Hargrett, NT, Blake, PA and Cohen, ML (1983). Hemorrhagic colitis associated with a rare Escherichia coli serotype. New England Journal of Medicine 308: 681–685.Google Scholar
Russo, TA and Johnson, JR (2003). Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes and Infection 5: 449–456.Google Scholar
Samuel, G and Reeves, P (2003). Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydrate Research 338: 2503–2519.Google Scholar
Scheutz, F, Cheasty, T, Woodward, D and Smith, HR (2004). Designation of O174 and O175 to temporary O groups OX3 and OX7, and six new E. coli O groups that include verocytotoxin-producing E. coli (VTEC): O176, O177, O178, O179, O180 and O181. APMIS 112: 569–584.Google Scholar
Smith, JL, Fratamico, PM and Gunther, N (2007). Extraintestinal pathogenic Escherichia coli (ExPEC). Foodborne Pathogens and Disease 4: 134–163.Google Scholar
Stenutz, R, Weintraub, A and Widmalm, G (2006). The structures of Escherichia coli O-polysaccharide antigens. FEMS Microbiology Review 30: 382–403.Google Scholar
Stromberg, ZR, Baumann, NW, Lewis, GL, Sevart, NJ, Cernicchiaro, N, Renter, DG, Marx, DB, Phebus, RK, Moxley, RA (2015). Prevalence of enterohemorrhagic Escherichia coli O26, O45, O103, O111, O121, O145, and O157 on hides and preintervention carcass surfaces of feedlot cattle at harvest. Foodborne Pathogens and Disease 12: 631–638.Google Scholar
Sura, R, Van Kruiningen, HJ, DebRoy, C, Hinckley, LS, Greenberg, KJ, Gordon, Z and French, RA (2007). Extraintestinal pathogenic E. coli (ExPEC) induced acute necrotizing pneumonia in cats. Zoonoses and Public Health 54: 307–313.Google Scholar
Tseng, M, Fratamico, PM, Bagi, L, Delannoy, S, Fach, P, Manning, SD and Funk, JA (2014). Diverse virulence gene content of Shiga toxin-producing Escherichia coli from finishing swine. Applied and Environmental Microbiology 80: 6395–6402.Google Scholar
Wang, L and Reeves, PR (1998). Organization of Escherichia coli O157 O antigen gene cluster and identification of its specific genes. Infection and Immunity 66: 3545–3551.Google Scholar
Wang, Q, Ruan, X, Wei, D, Hu, Z, Wu, L, Yu, T, Feng, L and Wang, L (2010). Development of a serogroup-specific multiplex PCR assay to detect a set of Escherichia coli serogroups based on the identification of their O-antigen gene clusters. Molecular and Cellular Probes 24: 286–290.Google Scholar