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Shiga Toxin 2F-Producing Escherichia Albertii from a Symptomatic Human

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Shiga Toxin 2F-Producing Escherichia Albertii from a Symptomatic Human Jpn. J. Infect. Dis., 67, 204-208, 2014 Short Communication Shiga Toxin 2f-Producing Escherichia albertii from a Symptomatic Human Koichi Murakami1*, Yoshiki Etoh1, Eri Tanaka2, Sachiko Ichihara1, Kazumi Horikawa1, Kimiko Kawano3,TadasukeOoka4, Yoshiaki Kawamura2, and Kenitiro Ito5 1Fukuoka Institute of Health and Environmental Sciences, Fukuoka 818-0135; 2Department of Microbiology, School of Pharmacy, Aichi Gakuin University, Aichi 464-8650; 3Miyazaki Prefectural Institute for Public Health and Environment, Miyazaki 889-2155; 4Division of Microbiology, Department of Infectious Diseases, Faculty of Medicine, University of Miyazaki, Miyazaki 889-1692; and 5National Institute of Infectious Diseases, Tokyo 162-8640, Japan (Received August 15, 2013. Accepted November 18, 2013) SUMMARY: The previously identified Shiga toxin (Stx) 2f-producing Escherichia coli O115:HNM strain F08/101-31, isolated from a symptomatic human, was confirmed to be E. albertii in the present study by whole genome DNA–DNA hybridizations, by sequencing (cpn60, dnaJ, and 16S rRNA genes), and by multi-locus sequence typing. The F08/101-31 strain was originally identified as E. coli rather than the relatively new bacterial species E. albertii, which was first described in 2003, because it did not display any of the biochemical characteristics of E. albertii. This new classification will impact public health management strategies in Japan because the present study showed that some E. albertii strains, which are often misidentified as E. coli, produce Stx and likely cause diarrhea in humans. Therefore, further guidelines for the management and identification of Stx-producing E. albertii are required in Japan. The discovery of Shiga toxin (Stx)-producing Es- nome DNA–DNA hybridization and DNA sequencing cherichia albertii strains was significant from a public techniques. The purpose of this study was to describe health perspective in Japan (1). E. albertii was first de- the characteristics of the E. albertii strain for the benefit scribed by Huys et al. in 2003 (2). This newly described of public health. enteropathogen is often misidentified as E. coli (3) or For genetic analysis, species-specific PCR analysis, other members of the family Enterobacteriaceae be- whole-genome DNA–DNA hybridization, sequence cause of its poorly defined biochemical characteristics analysis (16S rRNA genes, cpn60 (groEL), and dnaJ), and general obscurity. In addition, E. albertii closely and multi-locus sequence typing (MLST) were per- resembles E. coli in its phenotypic characteristics. formed. The F08/101-31 strain was examined by Retention of the major virulence factor intimin in E. al- species-specific PCR, as described previously, for the bertii is well established (4,5), whereas little is known presence of E. albertii-specific sequences within lysP about the incidence of Stx-producing E. albertii (1). Stxs and mdh (4) and for E. coli, Shigella,andE. albertii/S. are the most significant virulence factors of Stx-produc- boydii lineage-detecting alleles of clpX (4,8). Whole-ge- ing E. coli (STEC) in human infections. However, nome DNA–DNA hybridizations were performed be- STEC strains that produce intimin, a host-cell adhesin, tween the F08/101-31 strain and the E. albertii type often cause more critical symptoms in patients than strain LMG 20976T as well as other strains of closely STEC strains that do not produce intimin (6). There- related species (E. coli JCM 1649T and Hafnia alvei fore, the misidentification of Stx-producing E. albertii JCM 1666T). DNA extraction and purification were per- strains that also produce intimin as E. coli may compli- formed as described by Marmur (9) and Boom et al. cate public health monitoring strategies in many coun- (10), respectively. A membrane-filter DNA–DNA tries. hybridization method was performed as described by The F08/101-31 strain, which was previously reported Tourova and Antonov (11). Photobiotin-labeled DNA as Stx2f-producing E. coli O115:HNM harboring eae was hybridized with filter-bound DNA in 6× standard (7), was recently inferred to be an Stx2f-producing E. al- saline citrate and 50z formamide at 359C (optimal con- bertii strain on the basis of species-specific polymerase dition) and 459C (stringent condition). The amount of chain reaction (PCR) analysis (4,8). Therefore, in the re-associated DNA was measured using Image Quant present study, we attempted to definitively determine LAS4000 (GE Healthcare Bioscience, Tokyo, Japan), whether the strain is an E. albertii isolate by whole-ge- followed by the addition of alkaline phosphatase-conju- gated streptavidin and chemiluminescence substrate *Corresponding author: Mailing address: Fukuoka Institute (CDP-star; Roche Applied Science, Tokyo, Japan) to of Health and Environmental Sciences, 39 Mukaizano, the filters. The amplification and sequencing of 16S Dazaifu, Fukuoka 818-0135, Japan. Tel: ＋81-92-921- rRNA genes, cpn60 (groEL), and dnaJ were performed 9944, Fax: ＋81-92-928-1203, E-mail: murakami＠fihes. as follows: the 16S rRNA genes (1483 bp) were se- pref.fukuoka.jp quenced using previously described primers (12), and 204 E. albertii with Stx2f from a Symptomatic Human 1352 bp of the resultant sequences were compared with of phenotypic assays using both conventional methods corresponding regions from other bacterial species from and a commercial test strip (Table 1). The strain was ex- the DNA Data Bank of Japan (DDBJ) using a the Basic amined for indole production, Voges–Proskauer reac- Local Alignment Search Tool (BLAST) (http://blast. tion, motility at 359C, presence of lysine decarboxylase ddbj.nig.ac.jp/blastn?lang＝ja). Partial sequences of and ornithine decarboxylase, acetate utilization, and gas cpn60 (590 bp) were amplified as described previously production from D-glucose, as described previously (http://homepage.usask.ca/ Ã jeh369/cpn60 _ universal _ (18). Other phenotypic characteristics of the strain were primers.html, accessed June 2012), along with those of tested using API 20E and API 50 CH test strips (bio- dnaJ (554 bp) (13). The amplified sequences were then Máerieux, Ltd., Marcy-l' ÁEtoile, France), according to compared with corresponding sequences from other the manufacturer's instructions. related species listed in DDBJ using BLAST analysis. Genotyping analysis by species-specific PCR revealed MLST analysis was performed as described previously that the F08/101-31 strain exhibited E. albertii-specific (14) using the housekeeping genes adk, fumC, gyrB, icd, bands for lysP (252 bp) and mdh (115 bp). The DNA– mdh, purA,andrecA. Allele sequences for each strain DNA hybridization values obtained under optimal were then concatenated in the order adk–fumC–gyrB– (359C) and stringent (459C) conditions are shown in Ta- icd–mdh–purA–recA to obtain a final composite length ble 2. The values for the F08/101-31 strain and the E. of 3423 bp and analyzed as described previously (14). albertii control strain LMG 20976T were almost identi- Further genotypic analysis of the F08/101-31 strain cal, indicating that F08/101-31 is an E. albertii strain, was performed as detailed below, along with intimin with a hybridization value of À70z obtained even un- typing. In brief, the genes lpfAO26, sfpA,EHEC-hlyA, der stringent conditions. Sequences comparison of the irp2,andfyuA were amplified using primers described 16S rRNA genes, cpn60,anddnaJ of the F08/101-31 by Sonntag et al. (15), and the cytolethal distending tox- strain with those of other related strains revealed that in gene (cdt) was amplified according to the method de- F08/101-31 was more similar to E. albertii than other scribed by Pickett et al. (16). The intimin gene (eae) species (Fig. 1). Only 8 out of 1352 bp of the 16S rRNA from the F08/101-31 strain was subtyped using gene sequence differed between the F08/101-31 strain heteroduplex mobility analysis, as described previously and E. albertii LMG 20976T (Fig. 1). On the other hand, (17). BLAST analysis revealed a mismatch of 20 bp between The F08/101-31 strain was compared with known E. the 16S rRNA gene sequences of the F08/101-31 strain albertii isolates LMG 20976T and LMG 20973 in a series and E. coli ATCC 1352T, its closest relative among non- Table 1. Biological characteristics of F08/101-31 and other E. albertii strains tested or cited from the literature Characteristic described C) Strain or species 9 -Glucose, gas -Mannitol, acid -Sorbitol, acid -Xylose, acid -Arabinose, acid -Arabitol, acid -Rhamnose, acid Cellobiose, acid Dulcitol, acid Lactose, acid Sucrose, acid Adonitol, acid Raffinose, acid Indole production (24 h) Voges-Proskauer Motility (35 D L L D L D D Lysine decarboxylase Ornithine decarboxylase Acetate use (48 h) F08/101-31 ＋ －－＋ ＋ ＋ ＋－＋－－－－－＋－－＋－ E. albertii LMG20976T and LMG20973 － －－＋ ＋ ＋ ＋－＋－－－－－＋－－－－ E. albertii (biogroup 1)1) 0z2) 0z 0z 100z 100z 40z 100z 0z 100z 0z 0z 0z 0z 0z 100z 0z 0z 100z 0z E. albertii (biogroup 2)1) 100z 0z 0z 0z 100z 0z 40z 0z 100z 0z 0z 0z 0z 0z 100z 0z 0z 0z 0z 1): Cited from ref. 19. 2):0z, percentage of positive strains. Table 2. DNA–DNA hybridization values DNA hybridization (z) with biotin-labelled DNA from: Escherichia albertii Escherichia coli T Strain F08/101-31 LMG 20976T JCM1649T Hafnia alvei JCM1666 Optimal1) Stringent2) Optimal Stringent Optimal Stringent Optimal Stringent F08/101-31 100 ± 0100± 0 79.7 ± 5.9 73.7 ± 2.4 55.6 ± 3.8 57.5 ± 1.4 12.0 ± 4.7 7.2 ± 1.6 Escherichia albertii LMG20976T 82.6 ± 6.8 80.6 ± 3.7 100 ± 0100± 057.9± 3.3 44.1 ± 1.0 4.4 ± 1.6 7.7 ± 3.2 Escherichia coli JCM1649T 52.9 ± 2.7 35.9 ± 4.4 59.0 ± 0.4 50.8 ± 5.0 100 ± 0 100 ± 010.8± 1.4 5.5 ± 2.4 Hafnia alvei JCM1666T 5.0 ± 0.4 8.7 ± 0.3 8.4 ± 5.6 5.3 ± 1.9 8.6 ± 0.4 3.4 ± 0.8 100 ± 0100± 0 1): Under optimal hybridization condition (359C).
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