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Antimicrobial Agents and Chemotherapy, April 2009, p. 1630-1635, Vol. 53, No. 4
0066-4804/09/$08.00+0     doi:10.1128/AAC.01431-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

blaCTX-M Genes in Escherichia coli Strains from Croatian Hospitals Are Located in New (blaCTX-M-3a) and Widely Spread (blaCTX-M-3a and blaCTX-M-15) Genetic Structures{triangledown}

Elzbieta Literacka,1 Branka Bedenic,2 Anna Baraniak,1 Janusz Fiett,1 Marija Tonkic,3 Ines Jajic-Bencic,4 and Marek Gniadkowski1*

National Medicines Institute, Warsaw, Poland,1 School of Medicine, University of Zagreb, and Clinical Hospital Center, Zagreb, Croatia,2 University Hospital, Split, Croatia,3 Sisters of Mercy University Hospital, Zagreb, Croatia4

Received 24 October 2008/ Returned for modification 28 December 2008/ Accepted 25 January 2009


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ABSTRACT
 
CTX-M-producing Escherichia coli isolates from three Croatian hospitals were analyzed. All blaCTX-M-15 genes and one blaCTX-M-3a gene resided in widely spread ISEcp1 transposition modules, but other blaCTX-M-3a genes were in a new configuration with two IS26 copies, indicating a new event of gene mobilization from a Kluyvera ascorbata genome. The study confirmed the role of the E. coli ST131 clonal group with IncFII-type plasmids in the spread of blaCTX-M-15 and of IncL/M pCTX-M3-type plasmids in the dissemination of blaCTX-M-3a.


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INTRODUCTION
 
The rapid spread of CTX-M extended-spectrum β-lactamases (ESBLs) has been one of the recent spectacular changes in ESBL epidemiology (7, 9, 24, 32). CTX-Ms are derivatives of Kluyvera species β-lactamases (7, 29, 32), and mobilization of blaCTX-M genes has occurred frequently (4), with the essential assistance of ISEcp1 and ISCR1 elements, commonly found at their 5' flanks (29, 32). These elements may transpose with downstream DNA fragments, which in the case of ISEcp1 requires an alternative inverted right repeat (IRR) to form the 3' end of the transposition module (29). Such IRRs are behind β-lactamase genes in Kluyvera ascorbata chromosomes, including one inside orf477, which follows the β-lactamase genes directly (22, 31). Structure details of the modules, like the ISEcp1-blaCTX-M distance and the 3'-end position, are markers of particular mobilizations. More flexible are the plasmids in which they reside; however, it seems that successful dissemination of some blaCTX-M variants greatly depends on their locations on specific molecules of different incompatibility groups (13, 17, 18, 27). The blaCTX-M-15 gene is linked to IncFII or IncI1 plasmid families worldwide (13, 18, 27), while the diffusion of blaCTX-M-3 was attributed to IncL/M, IncN, or IncA/C plasmids (3, 6, 17, 18, 27, 33). The most recent data also underline the role of the spread of particular clones, mostly of Escherichia coli clones with CTX-M-15 (23, 40).

This study revealed a high diversity of the context of blaCTX-M-3/-15 genes in E. coli from Croatia and confirmed the importance of specific clones and plasmid types in their spread.

Eleven E. coli isolates were identified between 2002 and 2005 in three hospitals: the Clinical Hospital Center in Zagreb, Croatia (center Z1) (n = 5); the Sisters of Mercy Hospital in Zagreb (center Z2) (n = 1); and the University Hospital in Split, Croatia (center S) (n = 5) (Table 1). The partial data for isolates from center S were published previously (38). The all isolates tested positive for ESBLs by the double-disk test (19). MICs of β-lactams, determined by broth microdilution according to the CLSI guidelines (12), showed typical ESBL-mediated patterns, with some variation between centers (Table 2). Conjugation was performed as described previously (16), with E. coli A15 Rifr as a recipient and cefotaxime (2 µg/ml) and rifampin (rifampicin) (256 µg/ml) as selection agents. Transfer of resistance to non-β-lactams was tested by disk diffusion (12). All isolates from center Z1 produced transconjugants with ESBLs and resistance to aminoglycosides, co-trimoxazole, and tetracycline (Table 1), differing from transconjugants of isolates from center S (38). Isolate 49 from center Z2 did not mate.


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  		TABLE 1. Typing, β-lactamase content, plasmid characteristics, and blaCTX-M gene contexts of the study isolates


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  		TABLE 2. Antimicrobial susceptibilities of clinical isolates

The isolates were classified into major E. coli phylogroups by using the PCR-based approach (11). All isolates from centers Z1 and Z2 and two from center S (isolates 32 and 86) were classified in the virulent phylogroup B2, while the remaining isolates from center S were classified into the commensal phylogroup A (Table 1). Pulsed-field gel electrophoresis (PFGE) was performed as described by Kaufmann (21) and interpreted according to the guidelines of Tenover et al. (37). All isolates from center Z1 produced identical XbaI PFGE patterns (Table 1), while of the others, only the two B2 isolates from center S, 32 and 86, were related to each other, as shown previously (38). Representative isolate 52 from center Z1 and all isolates from hospitals Z2 and S were analyzed by multilocus sequence typing (39); the Internet database (www.mlst.net) was used for assigning sequence types (STs). These isolates had different STs (Table 1), all of which were new combinations of known alleles. The only similar allelic profiles were those of the related B2 isolates 32 and 86 (ST1038 and ST1039, respectively). Some STs were single-locus variants of STs found previously, with ST1035 of isolate 52 from center Z1 being a single-locus variant of ST131. Accumulating data document the global spread of the E. coli ST131 clone with CTX-M-15, observed so far in nine countries in Europe, North and South America, and Asia (13; www.mlst.net). The Croatian outbreak strain from center Z1 seems to represent the same pandemic lineage.

β-Lactamases were profiled by isoelectric focusing, as described previously (5). All isolates from center Z1 and their transconjugants produced β-lactamases with pIs of 8.9 and 7.4, while those from hospitals S and Z2 had enzymes with a pI of 8.4 (Table 1). β-Lactamases with a pI of 5.4 were found in some isolates from center S and in one transconjugant of these isolates (isolate 100). The blaCTX-M genes were amplified with primers P1C and P2D (Table 3) (16) and sequenced as reported previously (3). The pI 8.9 β-lactamases were CTX-M-15 (20), and the pI 8.4 enzymes were CTX-M-3, specified by the blaCTX-M-3a allele (16, 41). CTX-M-3 and especially CTX-M-15 belong to predominant CTX-M types in Europe (9, 24, 32).


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  		TABLE 3. Selected primers used in the study

Plasmid DNA was purified (Plasmid Midi kit; Qiagen, Hilden, Germany) from the transconjugant of isolate 52 from center Z1, from transconjugants of all isolates from center S, and from isolate 49 from center Z2. In PCRs, total DNAs of the other transconjugants from center Z1 were included. Plasmid preparations contained single large molecules. For fingerprinting, they were digested with PstI (Fermentas, Vilnius, Lithuania). Four fingerprints were observed (Table 1): pattern D for the isolate from center Z1 (~150 kb) and patterns A, B, and C for the isolates from center S (the plasmid of the center Z2 isolate degraded). PCR-based replicon typing (PBRT), limited to replicons F1A, F1B, FII, I1, and L/M, was performed according to the method of Carattoli et al. (10). Replicons FII and FIA were detected in plasmids of center Z1 isolates, while among isolates from hospital S, replicon FII correlated with fingerprint A and replicon L/M with B and C (Table 1). None of the replicons tested was found in the center Z2 isolate. The β-lactamase genes blaTEM-1 and blaOXA-1 were identified by PCR (25, 35) (Table 3). The aminoglycoside and quinolone resistance gene aac(6')-Ib-cr (30) was detected with primer qac2 (1) and two primers with variant 3' nucleotides, qac3-Ib and qac3-Ib-cr (Table 3); a positive result was obtained with qac2 and qac3-Ib-cr. Plasmids of center Z1 isolates carried blaOXA-1 and aac(6')-Ib-cr, whereas that of isolate 100 from hospital S contained blaTEM-1 (Table 1). The results obtained indicated that the blaCTX-M-15 gene of the outbreak isolates from center Z1 was located on a plasmid(s) similar to plasmids observed worldwide [replicons FII and FIA, blaOXA-1, aac(6')-Ib-cr, resistance to co-trimoxazole and tetracycline] (13, 18, 27). The plasmid with blaCTX-M-3a in isolate 100 from hospital S resembled plasmids spreading in Poland (pCTX-M3-type) and Bulgaria (replicon L/M, blaTEM-1, resistance to aminoglycosides and co-trimoxazole) (3, 17, 33).

The presence of ISEcp1 and IS26 was studied by PCR and hybridization. The elements were amplified with primers ISEcp1L1 and ALA-5 and primers IS26LF and IS26RR, respectively (Table 3). In hybridization, the blaCTX-M-3a/15 genes were included as well. PstI-digested plasmid DNA was blotted onto a Hybond-N+ membrane and hybridized sequentially with blaCTX-M, IS26, and ISEcp1 probes (34), using the ECL labeling and detection system (Amersham Biosciences, Little Chalfont, United Kingdom). ISEcp1 was identified in plasmids of all isolates from center Z1 and only in isolate 100 from center S of the others, and the ISEcp1 and blaCTX-M probes hybridized to single and the same PstI bands (results not shown). The IS26 PCR was positive with each DNA, and all plasmids tested had multiple bands hybridizing with the IS26 probe. In plasmids of isolates 16, 32, 36, and 86 from center S, IS26 hybridized to bands of ~4.5 kb which also contained their blaCTX-M-3a genes.

The location of ISEcp1 upstream from blaCTX-M-3a/-15 genes was analyzed for all isolates containing ISEcp1 with primers ALA-4 and ALA-3 (2) and sequencing of the amplicons. The 3' ends of the transposition modules were mapped with primer P1A (2) and two reverse primers hybridizing with K. ascorbata orf477 (Table 3; Fig. 1). Primer orf477-IRR matches the alternative ISEcp1 IRR, whereas orf477-27 anneals just further downstream (from blaCTX-M) (17, 31). In isolates from center Z1, ISEcp1 was distant by 49 bp from blaCTX-M-15, while in isolate 100 from center S, it resided 128 bp from blaCTX-M-3a. In the mapping of the 3' ends, only the PCR with primers P1A and orf477-IRR worked in all these cases, indicating that both modules terminated at the ISEcp1 IRR within orf477. The blaCTX-M-15 gene of the outbreak isolates from center Z1 was located in the structure (Fig. 1) originally identified in the IncFII plasmid pC15-1a from Canada (8) and later in other studies (14, 24, 27). The module with blaCTX-M-3a in isolate 100 from center S was identical to the mobile element of pCTX-M3-type plasmids in Poland (3, 17) and seen also in France (14) (Fig. 1).


Figure 1
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  		FIG. 1. Schematic representation of the genetic structures identified in the study: the ISEcp1-blaCTX-M-15 (top) and ISEcp1-blaCTX-M-3a (middle) transposition modules and the IS26-blaCTX-M-3a-IS26 element (bottom). The structures of the ISEcp1 modules are based on the sequence data from references 8 and 17. The scheme of the IS26-associated locus is based on sequences of the plasmidic PstI fragments (4,553 bp) cloned in this work. The double horizontal bar indicates a fragment homologous to K. ascorbata DNA (31), while the single thick bar indicates a fragment homologous to the A. baumannii AYE sequence (15). The broken line used to draw the arrow of the transposase pseudo-ORF symbolizes its disruption by the nonframe deletion. Striped boxes refer to the IRL and IRR segments of IS26 and ISEcp1 elements, respectively, including the alternative ISEcp1 IRR located within K. ascorbata orf477 (in the IS26-associated structure shown only for the comparison of {Delta}orf477 fragments in the modules). Black triangles refer to ATG codons of blaCTX-M and IS26 tnpA genes. PCR primers shown in the diagrams are those that were used for PCR mapping of the blaCTX-M-carrying modules.

The results shown above and previously (38) suggested that in most of the isolates from center S, the blaCTX-M-3a genes were linked to the IS26 element(s). The ~4.5-kb PstI plasmid fragments of isolates 16, 32, and 86, hybridizing with IS26 and blaCTX-M probes, were cloned in vector pHSG398 (36). E. coli DH5{alpha} transformants were selected with 2 µg/ml cefotaxime and 25 µg/ml chloramphenicol. The entire inserts were sequenced by primer walking; sequences were analyzed with the Lasergene version 7.1.0 software (DNAStar, Madison, WI) and the NCBI BLASTn option (www.ncbi.nlm.nih.gov). The three fragments had identical sequences, with parts of IS26 elements at each end (PstI cuts at one site inside IS26). The structure of the locus is shown in Fig. 1. The IS26-1 and IS26-2 elements are directed outside the locus. Upstream from IS26-1 there is a 1,362-bp region identical to a chromosomal fragment of K. ascorbata strain 69 with blaCTX-M-3a (31). The blaCTX-M-3a coding sequence starts 69 bp upstream from IS26-1 and is followed by a 372-bp fragment of orf477. The remaining 3,032-bp region is homologous to a fragment of a large resistance island in the Acinetobacter baumannii AYE strain (GenBank accession no. CT025832) (15), containing an open reading frame (ORF) of a putative transposase (position 69382..72822) that overlaps an oppositely oriented IS26 (position 69153..69972). The cloned plasmidic sequence lacked the 3' part of IS26-2 (661 bp) with the 5' end of the ORF (432 bp). The transposase ORF-like region differs by 81 nucleotides and by having a 10-bp deletion from the corresponding part of the AYE sequence (97.0% identity), which causes frameshifting and a nonsense mutation, shortening the ORF by 918 of 1,147 codons. Two other homologous sequences matched fragments located downstream of the deletion and not overlapping IS26. These were the Tn1000-like transposase ORF (1,209 bp [96.8% identity]) from the vicinity of the blaCTX-M-10 gene (28) and the Tn5394 transposase gene from plasmid pEP36 (2,740 bp [76.7% identity]) (26). Four pairs of primers (Table 3; Fig. 1) were used for PCR mapping of the loci in the remaining isolate from center S (isolate 36) and in isolate 49 from center Z2, showing the same structure in both isolates.

The IS26-blaCTX-M-3a-IS26 module of the isolates from center S and center Z2 is the first case of a blaCTX-M gene flanked by two IS26 copies. Such configurations are usually mobile (29), which probably also applies to this module residing in different plasmid platforms. It is difficult to judge whether blaCTX-M-3a was originally mobilized by IS26 or, e.g., by ISEcp1 followed by secondary IS26 insertions like those in some other blaCTX-M-3a or blaCTX-M-15 genes (14, 40). However, this blaCTX-M-3a gene was mobilized in an event other than those reported so far. It could not have arisen from the pCTX-M3 ISEcp1-blaCTX-M-3a module because the K. ascorbata DNA continues 27 bp beyond the orf477 ISEcp1 IRR or from the module described in Spain, where ISEcp1 is placed 46 bp from blaCTX-M-3a (27). Therefore, the known blaCTX-M-3a genes arose from at least three mobilizations, strengthening the earlier observation of frequent blaCTX-M escapes from Kluyvera genomes (4). The significance of the transposase pseudo-ORF remains unknown. It might have had transposition functions; however, it is difficult to reveal when and how it was assembled with blaCTX-M-3a and whether it played any role in the gene's mobilization or spread.


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Nucleotide sequence accession number.
 
The nucleotide sequence of the IS26-blaCTX-M-3a-IS26 locus of isolate 16 will appear in the EMBL database under accession no. FM213371.


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ACKNOWLEDGMENTS
 
We thank A. Bauernfeind for the E. coli A15 strain and J. Empel for helpful discussions.

This work was part of the activities of the MOSAR integrated project (LSHP-CT-2007-037941) supported by the European Commission within the 6th Framework Programme (E.L., A.B., J.F., and M.G.).


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FOOTNOTES
 
* Corresponding author. Mailing address: National Medicines Institute, ul. Chelmska 30/34, 00-725 Warsaw, Poland. Phone: (48) 22-851 43 88. Fax: (48) 22-841 29 49. E-mail: gniadkow{at}cls.edu.pl Back

{triangledown} Published ahead of print on 2 February 2009. Back


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Antimicrobial Agents and Chemotherapy, April 2009, p. 1630-1635, Vol. 53, No. 4
0066-4804/09/$08.00+0     doi:10.1128/AAC.01431-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.



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