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Applied and Environmental Microbiology, August 2005, p. 4941-4944, Vol. 71, No. 8
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.8.4941-4944.2005

SHORT REPORT

Molecular Serotyping of Escherichia coli O26:H11

Lisa M. Durso, James L. Bono, and James E. Keen*

USDA, ARS, U.S. Meat Animal Research Center, P.O. Box 166, State Spur 18D, Clay Center, Nebraska 68933

Received 29 October 2004/ Accepted 14 March 2005


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ABSTRACT
 
Serotyping is the foundation of pathogenic Escherichia coli diagnostics; however, few laboratories have this capacity. We developed a molecular serotyping protocol that targets, genetically, the same somatic and flagellar antigens of E. coli O26:H11 used in traditional serotyping. It correctly serotypes strains untypeable by traditional methods, affording primary laboratories serotyping capabilities.


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INTRODUCTION
 
Human infections with Escherichia coli O26:H11 and O26:H-untypeable (H-) or H-nonmotile (NM) strains are associated with diarrhea, hemorrhagic colitis, and hemolytic uremic syndrome (2, 33). Depending on virulence factors, E. coli O26 is classified as enterohemorrhagic (EHEC) or enteropathogenic (EPEC). The E. coli O26 serotype, first reported to cause pediatric EPEC diarrhea (18), has been isolated from EHEC outbreaks in Europe (1, 13, 15, 31), South America (22, 28), and Japan (10, 11); from sporadic cases in Canada (12), Australia (7), and the United States (4); and from sick (14, 21) and healthy (20, 25, 32) livestock. E. coli O26 is the most frequently isolated non-O157 Shiga-toxigenic E. coli (STEC) associated with human clinical illness (3), and E. coli O26:H11 is the clinically most important and epidemiologically most predominant EPEC and EHEC O26 serotype (2, 33).

Conventional E. coli O:H serotyping by agglutination of somatic and flagellar antigens by the use of anti-E. coli polyclonal antiserum is time consuming, expensive, and available only in a small number of reference laboratories (3, 33). E. coli O:H serotyping of pathogens may be required, however, for proper diagnosis and treatment, to maximize an isolate's usefulness for surveillance and to determine overall disease trends (33). PCR-based methodologies to detect or identify pathogenic E. coli O26 strains have targeted virulence genes such as Shiga toxin (stx) (9) and intimin (eae) (12, 27), flagellar H-antigen genes fliC-fliA (17), and the O-antigen O26 wzx genes (5, 16, 23). PCR methods targeting O26 O-antigen or H11 fliC genes could substitute for serotyping (5, 24). We therefore developed a molecular serotyping method to target the somatic and flagellar antigens and to allow clinical laboratories to accurately serotype E. coli as O26 and/or H11 by multiplex PCR (mPCR).

A 12-kb region of the E. coli O26:NM O-antigen operon from bovine fecal isolate SB6629 was sequenced (accession number AY763106); this region is identical to the corresponding region of the O26 O-antigen operon sequence (AF529080) reported by D'Souza et al. (6). Twenty sets of E. coli O26 O-antigen specific primers were synthesized and evaluated against a small panel of E. coli O26 and non-O26 E. coli isolates. One primer set, wzx-wzyO26F and wzx-wzyO26R, targeting the O26 wzx-wzy genes (O-antigen flippase and polymerase, respectively), had 100% sensitivity and specificity and a suitable amplicon size.

The E. coli H7 flagellum gene sequence is heterogenous, and fliCH7 sequence of the O157 serogroup is distinct from fliCH7 sequence of other O serogroups (29). To determine H11 flagellum sequence heterogeneity across different O serogroups (35), the fliCH11 genes of 20 H11 E. coli isolates comprising five O serogroups were sequenced (accession numbers AY906918 to AY906937). Eighteen of these sequences were identical to those previously reported (34, 35). Two E. coli O26:H11 strains had one and two nonsynonymous substitutions, respectively, compared to the consensus fliCH11 sequence. Thus, we chose to use fliCH11 primers designed by Wang et al. (30) for our assay.

The primers for E. coli O26:H11 molecular serotyping were wzx-wzyO26F (5'-AAATTAGAAGCGCGTTCATC), wzx-wzyO26R (5'-CCCAGCAAGCCAATTATGACT), fliCRH11-1 (5'-ACTGTTAACGTAGATAGC) (30), and fliCRH11-2 (5'-TCAATTTCTGCAGAATATAC) (30). Cells were prepared by diluting overnight Trypticase soy broth cultures 1:10 with reagent grade water. The 20 µl PCR used 1 µl of template and 0.5 U HotStarTaq (QIAGEN, Valencia, CA). The PCR mix contained concentrations of 500 µM per nucleotide, 600 nM for each primer, and 4.5 mM MgCl2. Thermocycler conditions were 95°C for 15 min, 35 cycles of 94°C for 60 s, 56°C for 60 s, and 72°C for 60 s, and a final elongation of 72°C for 10 min. Amplicons were visualized by electrophoresis on a 2% agarose gel run at 100 V for 2 h, stained with ethidium bromide, and digitally photographed. Isolates positive for the O26 and H11 alleles displayed bands of 596 bp and 224 bp, respectively (Fig. 1). We applied the E. coli O26/H11 mPCR to three diverse bacterial isolate panels to evaluate assay performance. Panel I was composed of 344 isolates: 322 diverse E. coli of known O and/or H serotype (including 31 E. coli O26:H11 strains) of human, animal, insect, and environmental origins, and 22 non-E. coli. This panel was used to generate mPCR diagnostic sensitivity and specificity estimates. (A detailed list of the strains used is available at http://www.ars.usda.gov/sp2UserFiles/Place/54380570/AHRU/E.coli/AEM_Durso_isolate_list.pdf). The O26 and H11 serotype status of 42 E. coli strains comprising panel II was tested blindly (without knowledge of their conventional O:H serotype). Panel III, a subset of panel I composed of 35 E. coli O26:NM (34 eae positive, 1 eae negative) and 11 O26:H- (10 eae positive, 1 eae negative) strains, was used to estimate the proportion of E. coli O26:NM/H- strains that possess the fliCH11 gene without expressing the H11 antigen. Although all reactions were run in the multiplex format, assay performance was measured separately for the O26 and H11 primer sets. Additionally, E. coli O26 strains were serologically confirmed as O26 by enzyme immunoassay using an anti-E. coli O26 murine monoclonal antibody (26), and E. coli O26 and H11 strains were assayed for the presence of stx1, stx2, and eae genes as previously described (19) (Table 1).



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  		FIG. 1. Molecular serotyping of E. coli O26:H11 by multiplex PCR. Lane 1, molecular marker (100 bp); lane 2, H311b, O26 standard reference strain (E. coli O26:H11); lane 3, 5306-56 (E. coli O26:H46); lane 4, 88-4110 (E. coli O111:H11); lane 5, DEC 15C (E. coli O111:H21); lane 6, TWO7187a, O26 smooth (E. coli O26:H32); lane 7, TWO7187b, O26 rough (E. coli O26:H32); lane 8, 95.0256 (E. coli O26:H- untypeable); lane 9, TW04272 (E. coli O26:H nonmotile).


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  		TABLE 1. Sensitivity and specificity estimates of E. coli O26 and H11 mPCR compared to traditional serotyping for 344 panel I bacteria (322 E. coli and 22 non-E. coli)a

The E. coli O26/H11 mPCR assay was 100% sensitive and specific based on reactions with the 344 panel I bacteria (Table 1). The assay correctly determined the O26 and H11 serotype of the 42 blind-panel E. coli strains (Table 2). All 35 E. coli O26:NM and 10 of 11 E. coli O26:H- strains in panel III were fliCH11 positive. These results are consistent with the findings of Zhang et al. (34), who noted that eae-positive E. coli O26:H- strains belong to an H11 clonal complex. The fliCH11-negative E. coli O26:H- strain was eae negative and therefore not part of the H11 clonal complex. The mPCR assay also identified seven strains that had apparently been misserotyped or mislabeled with respect to O26 and/or H11 serotype. The mPCR and serotyping results for these seven strains initially appeared discordant. However, when these isolates were reserotyped by the E. coli Reference Center (University Park, PA), the revised results agreed with those of the mPCR O26/H11 assay. Importantly, molecular serotyping methods generate genotypic information, in contrast to traditional serotyping, which generates phenotypic (surface antigen expression) information. Thus, our E. coli O26/H11 mPCR permits serotyping of "antigenically silent" strains which are O or H untypeable by conventional serotyping techniques. For example, our PCR assay serotyped rough lipopolysaccharide (O-antigen-free) colonies of blind-panel isolate TW07187 as O26, and identified the fliCH11 gene in many NM and H- E. coli strains, in both O26 and non-O26 STEC.


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  		TABLE 2. Comparison of E. coli O26 and H11 serotyping results obtained from traditional serotyping, O26-specific monoclonal antibody enzyme-linked immunosorbent assay, and molecular serotyping by mPCR for 42 E. coli strains tested in a blind panel (panel II)

In conclusion, the E. coli O26/H11 mPCR assay accurately determined O26 and H11 serotypes of 364 conventionally serotyped E. coli strains by targeting the genes that encode the same somatic and flagellar antigens used in traditional serotyping. Furthermore, the mPCR assay serotyped E. coli isolates (such as rough O26 and nonmotile H11 strains) which were untypeable by conventional methods. Third, we found that 45 out of 46 STEC and non-STEC O26:NM/H- strains were fliCH11 positive, analogous to the case of STEC O157:NM strains, which almost always possess the fliCH7 gene (8). Finally, the assay allowed for confirmation of E. coli O26 and H11 serotype.

Traditional E. coli O:H serotyping, which detects surface antigen expression, will remain important, but application of molecular serotyping techniques that detect their genetic analogues (counterparts) have some relative advantages. While molecular E. coli O:H serotyping may not be appropriate for all bacteriologic investigations, it is well suited for clinical diagnostic, research laboratory, or epidemiologic investigations. The E. coli O26/H11 mPCR assay described here should allow laboratories to generate E. coli O26 and H11 serotype data using routine PCR techniques and readily available equipment, since few laboratories have the capacity for serotyping non-O157 STEC (33). The assay was designed to allow for the addition of other PCR targets, such as stx or eae. We optimized this assay for use with a pure bacterial culture; as with traditional serotyping, it is not appropriate for application to complex sample matrices with mixed microbial flora.


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Nucleotide sequence accession numbers.
 
The nucleotide sequence for E. coli O26 for the NM O-antigen operon from bovine fecal isolate SB6629 is deposited in GenBank as AY763106. Nucleotide sequences for 20 E. coli fliCH11 strains are as follows: strain ATCC 35401, O serotype 78, AY906918; strain DEC 10J, O serotype 70, AY906919; strain P1331, O serotype 26, AY906920; strain H311B, O serotype 26, AY906921; strain 89-491, O serotype 26, AY906922; strain 88-353, O serotype 26, AY906923; strain 88-157, O serotype 26, AY906924; strain H19, O serotype 26, AY906925; strain DEC 9E, O serotype 26, AY906926; strain DEC 9D, O serotype 26, AY906927; strain DEC 9A, O serotype 26, AY906928; strain DEC 10E, O serotype 26, AY906929; strain DEC 10D, O serotype 26, AY906930; strain DEC 10C, O serotype 26, AY906931; strain DEC 10B, O serotype 26, AY906932; strain Su 4321, O serotype 13, AY906933; strain 88-41, O serotype 111, AY906934; strain DEC 10A, O serotype 26, AY906935; strain DEC 8D, O serotype 26, AY906936; strain CL5, O serotype 26, AY906937.


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ACKNOWLEDGMENTS
 
This work was supported, in part, by USDA CSREES NRI grant 2002-2239 (awarded to J.E.K.). We thank Sandy Fryda-Bradley, Ron Mlejnek, and Liz Ossian for outstanding technical assistance; Kevin Tennill for photographic assistance; Joan Rosch for secretarial assistance; and Tom Wittum from The Ohio State University, Columbus, OH, Greg Siragusa from the USDA, ARS, Russell Research Center, Athens, GA, and anonymous reviewers for helpful comments on the manuscript. Bacterial isolates were kindly provided by C. Park, Inova Fairfax Hospital, Falls Church, VA; D. Francis, South Dakota State University, Brookings, SD; M. Doyle, University of Georgia, Athens, GA; D. Acheson, Food and Drug Administration, College Park, MD; J. Johnson, University of Minnesota Veterans Hospital, Minneapolis, MN; L. Riley, University of California, Berkeley, CA; T. Whittam, Michigan State University, East Lansing, MI; Centers for Disease Control and Prevention, Atlanta, GA; Texas Department of Health, Austin, TX; National Animal Disease Center, Ames, IA; and V. Lockary, State of Idaho Bureau of Laboratories, Boise, ID.

Product names are necessary to report factually on available data; however, the USDA neither guarantees nor warrants the standard of the product, and the use of the name by USDA implies no approval of the product to the exclusion of others that may also be suitable.


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FOOTNOTES
 
* Corresponding author. Mailing address: USDA, ARS, U.S. Meat Animal Research Center, P.O. Box 166, State Spur 18D, Clay Center, NE 68933. Phone: (402) 762-4343. Fax: (402) 762-4375. E-mail: keen{at}email.marc.usda.gov. Back


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Applied and Environmental Microbiology, August 2005, p. 4941-4944, Vol. 71, No. 8
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.8.4941-4944.2005




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  • Aktan, I., Carter, B., Wilking, H., La Ragione, R. M., Wieler, L., Woodward, M. J., Anjum, M. F. (2007). Influence of geographical origin, host animal and stx gene on the virulence characteristics of Escherichia coli O26 strains. J Med Microbiol 56: 1431-1439 [Abstract] [Full Text]  

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