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. 2007 Oct 12;73(24):8005–8011. doi: 10.1128/AEM.01325-07

Molecular Epidemiology of blaCMY-2 Plasmids Carried by Salmonella enterica and Escherichia coli Isolates from Cattle in the Pacific Northwest▿

Joshua B Daniels 1, Douglas R Call 1, Thomas E Besser 1,*
PMCID: PMC2168131  PMID: 17933916

Abstract

Restriction analyses of blaCMY-2-bearing plasmids and Salmonella and Escherichia coli hosts identified (i) shared highly similar plasmids in these species in rare cases, (ii) a clonal host-plasmid relationship in Salmonella enterica serotype Newport, and (iii) a very high diversity of strain types and plasmids among commensal E. coli isolates.

Nontyphoid Salmonella enterica subsp. enterica (NTS) causes approximately 36,000 confirmed cases of food-borne illness in the United States and an estimated 1.4 million unreported cases each year (9, 17, 25). A trend toward increasing antimicrobial resistance to broad-spectrum cephalosporins in some NTS serovars has raised concern because these drugs are regarded as first-line therapy in pediatric salmonellosis (11). The most recent surveillance data indicate that 0.6% of U.S. human NTS isolates are resistant to ceftriaxone and 3.4% are resistant to ceftiofur (a veterinary broad-spectrum cephalosporin) (7). The predominant mechanism of cephalosporin resistance in NTS in the United States is a cephamycinase encoded by plasmid-borne blaCMY-2 genes (11, 27, 28, 30). blaCMY-2, which likely originated from the chromosomal AmpC locus of Citrobacter freundii (1, 19), has been observed in plasmids in several species of the Enterobacteriacea (2-4, 15, 16, 18, 27, 29).

Commensal bacteria may serve as a reservoir of plasmid-borne antimicrobial resistance genes for pathogens, and there is evidence that plasmid transfer occurs readily between Escherichia coli and S. enterica. For example, a phylogenetic analysis of F plasmid-specific genes from reference collections of S. enterica and E. coli found several examples in which finO and traD sequence variants were shared between the two species (6). Furthermore, blaCMY-2 Southern blot experiments with plasmids from E. coli and S. enterica have revealed similarities among isolates, suggesting that sequences (in addition to the blaCMY-2 open reading frame) are shared among the plasmids harbored by these microbial genera (27, 28).

Cattle could represent an important niche for transfer of blaCMY-2 plasmids between E. coli and NTS. Both bacterial genera inhabit the bovine gastrointestinal tract, and selection pressure favoring cephalosporin resistance is ubiquitous in some cattle production systems due to the frequent use of ceftiofur (13). For example, between 2001 and 2003, the percentage of ceftiofur-resistant NTS rose more rapidly among isolates from U.S. cattle than in those from human, chicken, turkey, and swine hosts (8). The predominance of blaCMY-2--mediated cephalosporin resistance among NTS and E. coli isolates from cattle (20, 24, 30) led us to investigate the relationship between blaCMY-2 plasmids and the two microbial genera. Assessing the diversity of host chromosomal and plasmid DNAs from commensal isolates of E. coli and clinical isolates of S. enterica permitted us to evaluate whether blaCMY-2 dissemination in this ecological niche is clonal or due to epidemic plasmid spread and whether the nature of this process differed in a pathogen (S. enterica) and a potential reservoir of antimicrobial resistance genes (E. coli).

E. coli isolates from 46 animals originating in 14 herds and S. enterica isolates from 48 animals with salmonellosis originating in 47 herds were chosen to represent the bovine commensal flora and a major bovine pathogen, respectively. All isolates were obtained from cattle in Washington state or Idaho between 2001 and 2003. All isolates gave an amplicon of the appropriate length when tested by PCR using blaCMY-2-specific primers described by Zhao et al. (30) (Table 1).

TABLE 1.

blaCMY-2 containing S. enterica and E. coli isolates

Isolate Serotypea PFGE type Resistance phenotypeb
Plasmid type blaCMY-2 fragment size (kb)d Conjugativee Yr
Source strain Transformant
S8126 Dublin D1 AMP CHL GEN KAN SXT TET SSS STR CAZ Same as donorc 3 20 N 2003
S8133 Dublin D1 AMP CHL GEN KAN SXT TET SSS STR CAZ Same as donor 3 20 N 2002
S8244 Dublin D2 AMP CHL TET SSS STR CAZ Same as donor 7 20 N 2003
S8247 Dublin D1 AMP CHL GEN KAN TET SSS STR CAZ AMP CHL KAN TET SSS CAZ 3 20 Yf 2003
S8253 Dublin D2 AMP CHL TET SSS STR CAZ Same as donor 7 20 N 2003
S8274 Dublin D1 AMP CHL GEN KAN TET SSS STR CAZ Same as donor 3 20 N 2003
S8282 Dublin D3 AMP CHL GEN KAN TET SSS STR CAZ Same as donor 3 20 N 2002
S7651 Muenster M1 AMP CHL GEN KAN SXT TET SSS STR CAZ Same as donor 2 3.2 N 2002
S7140 Newport N3 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7276 Newport N2 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7333 Newport N2 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7465 Newport N2 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7497 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7656 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7658 Newport N8 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7661 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7677 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7748 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7885 Newport N7 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7889 Newport N2 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7891 Newport N11 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7893 Newport N2 AMP TET SSS STR CAZ Same as donor 33 3.2 N 2002
S7894 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7906 Newport N10 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7909 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7918 Newport N13 AMP TET SSS STR CAZ Same as donor 31 3.2 N 2002
S7926 Newport N2 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7935 Newport N2 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S7936 Newport N12 AMP CHL GEN SXT TET SSS STR CAZ AMP CHL TET SSS CAZ 18 3.2 N 2002
S8118 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2002
S8124 Newport N3 AMP CHL TET SSS STR CAZ Same as donor 32 3.2 N 2002
S8129 Newport N3 AMP CHL TET SSS STR CAZ Same as donor 13 20 N 2003
S8132 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2003
S8151 Newport N9 AMP CHL TET SSS STR CAZ Same as donor 13 20 N 2003
S8242 Newport N4 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2003
S8245 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2003
S8257 Newport N5 AMP TET SSS STR CAZ Same as donor 31 3.2 N 2003
S8258 Newport N1 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2003
S8277 Newport N4 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2003
S8280 Newport N2 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2003
S8281 Newport N2 AMP CHL TET SSS STR CAZ Same as donor 18 3.2 N 2003
S8912 Newport N6 AMP TET SSS STR CAZ Same as donor 30 3.2 N 2003
S8922 Newport N11 AMP TET SSS STR CAZ Same as donor 32 3.2 N 2003
S7655 Typhimurium T2 AMP CHL KAN SXT TET SSS STR CAZ Same as donor 14 20 N 2002
S7907 Typhimurium T4 AMP CHL KAN SXT TET SSS STR CAZ Same as donor 13 20 N 2002
S8238 Typhimurium T1 AMP CHL TET SSS STR CAZ Same as donor 29 3.2 N 2003
S8240 Typhimurium T5 AMP CHL KAN SXT TET SSS STR CAZ AMP CHL SXT TET SSS CAZ 11 20 N 2003
S8914 Typhimurium T3 AMP CHL KAN TET SSS STR CAZ Same as donor 13 20 N 2003
E1128 O2:H42 E23 AMP CHL TET SSS STR CAZ Same as donor 13 20 N 2002
E1216 O33:H4 E2 AMP CHL GEN SXT TET SSS STR CAZ AMP CHL SXT TET SSS CAZ 10 20 Y 2002
E1246 n:H30 E4 AMP CHL GEN KAN SXT TET SSS STR CAZ AMP CHL SXT TET SSS CAZ 13 20 Y 2002
E1291 O159:H4 E24 AMP CHL TET SSS STR CAZ Same as donor 10 20 Y 2001
E1445 O35:H16 E25 AMP CHL KAN SXT TET SSS STR CAZ Same as donor 24 20 Y 2001
E1455 O145:+ E26 AMP CHL GEN KAN TET SSS STR CAZ Same as donor 23 3.2 Y 2001
E1473 O35:H16 E27 AMP CHL KAN SXT TET SSS STR CAZ Same as donor 24 20 Y 2001
E2275 O66:H25 E28 AMP CHL GEN KAN SXT TET SSS STR CAZ Same as donor 1 3.2 N 2001
E2323 O154:H30 E13 AMP CHL KAN SXT TET SSS STR CAZ AMP CHL TET SSS CAZ 16 3.2 N 2002
E2331 n:H9 E29 AMP CHL TET SSS STR CAZ Same as donor 17 3.2 N 2002
E2346 O154:H30 E14 AMP CHL KAN SXT TET SSS STR CAZ AMP CHL TET SSS CAZ 17 3.2 N 2002
E2358 n:H42 E30 AMP CHL GEN KAN TET SSS STR CAZ Same as donor 23 3.2 N 2002
E2379 n:H48 E31 AMP CHL GEN KAN TET SSS STR CAZ Same as donor 24 3.2 N 2002
E2449 n:H42 E32 AMP CHL TET SSS STR CAZ Same as donor 13 20 Y 2002
E2469 O20:H30 E33 AMP CHL KAN SXT TET SSS STR CAZ Same as donor 20 20 Y 2002
E2517 n:H38 E34 AMP CHL GEN KAN SXT TET SSS STR CAZ Same as donor 5 3.2 Y 2002
E2530 O111:H8 E11 AMP CHL KAN SXT TET SSS STR CAZ AMP CHL SXT TET SSS CAZ 26 1 N 2002
E2588 n:H11 E19 AMP CHL GEN KAN SXT TET SSS STR CAZ AMP CHL GEN KAN TET SSS CAZ 19 20 N 2002
E2639 O8w:H16 E18 AMP CHL KAN TET SSS STR CAZ AMP CAZ 2 2.9 N 2002
E2654 n:H38 E35 AMP CHL KAN SXT TET SSS STR CAZ Same as donor 24 20 N 2002
E2676 O11:H15 E5 AMP CHL GEN KAN SXT TET SSS STR CAZ AMP CHL TET SSS CAZ 16 3.2 N 2002
E2679 n:H5or56 E20 AMP CHL GEN KAN SXT TET SSS STR CAZ AMP CHL GEN KAN TET SSS CAZ 21 3.2 N 2002
E2699 n:H28 E21 AMP CHL GEN KAN SXT TET SSS STR CAZ AMP CHL KAN SUL CAZ 22 20 Y 2002
E2713 n:H4 E15 AMP CHL KAN SXT TET SSS STR CAZ AMP CHL TET SSS CAZ 13 20 N 2002
E2759 O20:H18 E3 AMP CHL GEN KAN SXT TET SSS STR CAZ AMP CHL KAN SXT TET SSS CAZ 24 20 Y 2002
E2769 n:H4 E9 AMP CHL KAN SXT TET SSS STR CAZ AMP CHL SXT TET SSS CAZ 18 3.2 Y 2002
E525 O20:H30 E22 AMP CHL KAN SXT TET SSS STR CAZ Same as donor 20 20 Y 2002
E6875 O2:H42 E16 AMP CHL KAN SXT TET SSS STR CAZ AMP CHL TET SSS CAZ 17 3.2 N 2002
E6900 a:5or56 E12 AMP CHL GEN KAN SXT TET SSS STR CAZ AMP CHL GEN TET SSS CAZ 15 3.2 N 2003
E7119 O2:H42 E17 AMP CHL KAN SXT TET SSS STR CAZ AMP CHL TET SSS CAZ 15 3.2 N 2003
E7132 O116w:H9 E36 AMP CHL SXT TET SSS STR CAZ Same as donor 16 20 N 2003
E7140 O116w:H9 E37 AMP CHL TET SSS STR CAZ Same as donor 8 11, ∼20 N 2003
E7196 O101:H9 E6 AMP CHL GEN KAN SXT TET SSS STR CAZ AMP CHL TET SSS CAZ 10 20 Y 2002
E7212 n:H9 E7 AMP CHL GEN KAN TET SSS STR CAZ AMP CHL TET SSS CAZ 13 20 Y 2003
E7292 O117:H4 E8 AMP CHL GEN SXT TET SSS STR CAZ AMP CHL TET SSS CAZ 34 3.2 N 2003
E7403 O145:H12 E10 AMP CHL GEN KAN TET SSS STR CAZ AMP CHL GEN TET SSS CAZ 7 3.2, 11 N 2003
E793 O20:H30 E1 AMP CHL KAN SXT TET SSS STR CAZ AMP CAZ 6 3.2 Y 2003
E8100 O10:H42 E39 AMP CHL TET SSS STR CAZ Same as donor 27 1, 3.2 N 2003
E8142 n:H9 E41 AMP CHL SXT TET SSS STR CAZ Same as donor 13 20 Y 2003
E8166 n:H9 E42 AMP CHL SXT TET SSS STR CAZ Same as donor 10 20 N 2003
E8188 O159:H4 E43 AMP CHL TET SSS STR CAZ Same as donor 26 20 N 2003
E8430 O159:H4 E44 AMP CHL TET SSS STR CAZ Same as donor 26 20 N 2003
E8431 O159:H4 E45 AMP CHL TET SSS STR CAZ Same as donor 28 20 N 2003
E8603 n:n E46 AMP CAZ Same as donor 4 2.9, 4, 5 Y 2003
E8618 O159:H4 E38 AMP CHL TET SSS STR CAZ Same as donor 12 20 N 2003
E8625 O159:H4 E40 AMP CHL TET SSS STR CAZ Same as donor 25 20 N 2003
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a

n, negative; + positive, novel antigen; a, autoagglutination; w, weak agglutination.

b

AMP, ampicillin; CHL, chloramphenicol; GEN, gentamicin; KAN, kanamycin; SXT, sulfamethoxizone/trimethoprim; TET, tetracycline; STR, streptomycin; SSS, triple sulfa; CAZ, ceftazidime.

c

“Same as donor” is with respect to all resistances except streptomycin, as the recipient strain (DH10B) is intrinsically resistant to streptomycin.

d

A blaCMY-2-positive PstI fragment of 850 bp was present for all plasmids, in addition to the larger fragment reported in this column.

e

N, no; Y, yes.

f

Transconjugants were observed only when the helper plasmid pRK2013 was included in the mating mixture.

E. coli and S. enterica serotypes were determined by the Gastroenteric Disease Center (University Park, PA) and the National Veterinary Services Laboratory (Ames, IA), respectively. Isolates were assessed for pulsed-field gel electrophoresis (PFGE) type in accordance with PulseNet protocols (23). Plasmids were isolated by electroporation into E. coli DH10B and prepared for PstI restriction fragment length polymorphism (pRFLP) typing using previously described methods (12, 21). pRFLP typing and blaCMY-2 Southern blotting were performed as described by Giles et al. (12) but using continuous voltage (7.2 V/cm for 1.5 h). Agar diffusion susceptibility testing was performed in accordance with CLSI standards (10). Gel images were analyzed using Bionumerics (Applied Maths, Belgium) with optimization and tolerance settings determined by the minimum values required to classify a standard plasmid (which was included with each gel) as indistinguishable from itself in an unweighted pair group method with arithmetic mean (UPGMA) analysis.

S. enterica included four serotypes: Newport (n = 35), Typhimurium (n = 5), Dublin (n = 7), and Muenster (n = 1); PFGE patterns were highly similar within serotypes (Fig. 1). Sixteen serotypes were identified among the 28 E. coli isolates that were typeable for both O and H antigens, but PFGE patterns were markedly more diverse than in the Salmonella spp.; each of the 46 isolates displayed a unique pattern (data not shown). The differences in serotype and PFGE diversities between the two genera may reflect the sources of the isolates: clinical versus commensal bacteria from healthy animals. Pathogenic Salmonella spp. have been described as inherently clonal (5, 14), whereas relatively little is known about the genetic diversity of nonpathogenic E. coli isolates from animal sources. Winokur et al. found diverse PFGE patterns among 55 blaCMY-2 commensal E. coli isolates from clinical veterinary specimens (28). Taken together, these findings suggest that blaCMY-2-bearing commensal E. coli isolates are not strongly clonal at the serotype and PFGE levels, regardless of the clinical status of the source.

FIG. 1.

FIG. 1.

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UPGMA dendrograms with negative images of ethidium bromide-stained gels from XbaI PFGE of blaCMY-2-positive S. enterica from cattle following normalization and analysis with Bionumerics software. The PFGE type designations correspond to those referred to in Table 1. Ser., serotype.

Forty pRFLP patterns were observed among the 94 isolates; however, repeatability analyses using a subset of 14 plasmids demonstrated that consistent self-grouping was observed only at the 90% similarity level. Thus, we considered plasmids with ≥90% similarity indistinguishable, resulting in the designation of 34 unique patterns. Four reference plasmids (A, B, C, and D), described by Giles et al. (12), were included as positive controls. Twelve pRFLP patterns were observed in more than one bacterial isolate, and two patterns were observed in both genera, consistent with exchange of some plasmids among commensal E. coli and S. enterica isolates (Fig. 2). Eighty-five plasmids had blaCMY-2 Southern blot fragments identical to the A or C patterns previously described and were conserved within pRFLP types, consistent with horizontal-transfer activity (Fig. 3).

FIG. 2.

FIG. 2.

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UPGMA dendrogram with a negative image of an ethidium bromide-stained PstI plasmid RFLP gel after normalization in Bionumerics software. The bracketed strains indicate identical RFLP patterns from plasmids isolated from both E. coli and S. enterica. Plasmid type designations correspond to those in Table 1. Reference A, B, C, and D plasmids (12) were included as controls.

FIG. 3.

FIG. 3.

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(A) pRFLP of A, B, C, and D reference plasmids, followed by three examples of blaCMY-2 plasmids from S. enterica isolates from Washington state cattle. Lanes: 1, 8, and 12, 12-kb ladder; 2, λ\HindIII markers; 3, 4, 5, and 6, A, B, C, and D reference plasmids (12); 9, 10, and 11, pS7907, pS7909, and pS8129; 7, undigested reference plasmid D. (B) Southern hybridization of the gel from panel A with a full-length CMY-2 probe.

Each Salmonella serotype tended to be associated with a specific plasmid variant. Notably, for S. enterica serovar Newport, 26 of 35 isolates originated from 26 different herds but shared a single pRFLP type (type 18). Using the model of plasmid-bacterial-host associations proposed by Souza and Eguiarte (22), the relationship between S. enterica serovar Newport and its plasmids could be described as clonal, implying that blaCMY-2 plasmids in this serotype were largely disseminated with an epidemic host bacterium. In contrast, the diversity of plasmids from E. coli was high, reflecting the high level of PFGE and serotype diversity observed between the isolates. The exceptions to this observation were five pRFLP types (10, 13, 16, 17) associated with multiple serologically distinguishable host strains, consistent with the idea of epidemic plasmids (22).

Although there was evidence of interspecies sharing of plasmids, the predominance of only two plasmid variants (A and C) in Salmonella isolates from an animal niche containing a plethora of E. coli-borne plasmid variants (presumably available for transfer to Salmonella) was conspicuous, suggesting that the major mechanisms of blaCMY-2 dissemination differ between S. enterica and E. coli. This pattern is consistent with a recent study by Welch et al., who found greater diversity of plasmids among E. coli isolates than among the S. enterica isolates, using PCR primer sets representing 13 widely spaced loci from an entirely sequenced IncA/C blaCMY-2 plasmid from S. enterica serovar Newport (26). Our observation that isolates limited to a solitary niche (cattle) are similarly diverse suggests a model of blaCMY-2 dissemination in which insertions and deletions that occur during promiscuous plasmid sharing among E. coli isolates occasionally result in plasmids that are successful in a Salmonella host (such as pRFLP types 13 and 18). Also consistent with this model, conjugation experiments revealed that 40% of E. coli plasmids (versus 2% of Salmonella plasmids) were able to transfer or be mobilized to a Nalr DH5α recipient. The subsequent success of a Salmonella host/plasmid clone, then, is likely modulated by diverse factors, including virulence, infectivity, and environmental persistence, as well as antimicrobial selection pressures. Factors that promote interspecies exchange of antimicrobial-resistance plasmids and enhance dissemination of S. enterica clones merit further study.

Acknowledgments

We thank Mike Kahn, Min-Su Kang, and Yubei Zhang for their thoughtful discussions and technical assistance. Paul Fey at the University of Nebraska provided the “A, B, C, and D” plasmids.

This work was partially funded by USDA-NRI Epidemiological Approaches to Food Safety grant 2005-01373, NIAID NIH contract N01-AI-30055, and the Agricultural Animal Health Program, WSU College of Veterinary Medicine, Pullman, WA.

Footnotes

▿

Published ahead of print on 12 October 2007.

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