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Erratum: Kim, J.; et al. Characterization of mcr-1-Harboring Plasmids from Pan Drug-Resistant Escherichia coli Strains Isolated from Retail Raw Chicken in South Korea. Microorganisms 2019, 7, 344
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Erratum published on 18 October 2019, see Microorganisms 2019, 7(10), 470.
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Characterization of mcr-1-Harboring Plasmids from Pan Drug-Resistant Escherichia coli Strains Isolated from Retail Raw Chicken in South Korea

Department of Food and Animal Biotechnology, Research Institute for Agriculture and Life Sciences, Center for Food and Bioconvergence, Seoul National University, Seoul 08826, Korea
Department of Agricultural Biotechnology, Center for Food Safety and Toxicology, Seoul National University, Seoul 08826, Korea
Food-borne Pathogen Omics Research Center (FORC), Seoul National University, Seoul 08826, Korea
Beijing Advanced Innovation Center for Food Nutrition and Human Health, College of Veterinary Medicine, China Agricultural University, Beijing 100083, China
Environmental Health Sciences, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA
Authors to whom correspondence should be addressed.
Microorganisms 2019, 7(9), 344;
Received: 26 August 2019 / Revised: 5 September 2019 / Accepted: 11 September 2019 / Published: 12 September 2019


A number of studies from different countries have characterized mcr-1-harboring plasmids isolated from food; however, nothing has been reported about it in South Korea. In this study, we report the characterization of mcr-1 plasmids from pan drug-resistant (PDR) Escherichia coli strains isolated from retail food in the country. Colistin-resistant E. coli strains were isolated from retail raw chicken, and PCR was carried out to detect the mcr-1 gene. Whole genome sequencing of the mcr-1-positive strains was performed for further characterization. The results of whole genome sequencing revealed that all mcr-1 plasmids belonged to the IncI2 type. In addition to the mcr-1 plasmids, all of the isolates also carried additional plasmids possessing multiple antibiotic resistance genes, and the PDR was mediated by resistant plasmids except for fluoroquinolone resistance resulting from mutations in gyrA and parC. Interestingly, the mcr-1 plasmids were transferred by conjugation to other pathogenic strains including enterohemorrhagic E. coli (EHEC), enterotoxigenic E. coli (ETEC), enteroaggregative E. coli (EAEC), Salmonella, and Klebsiella at the frequencies of 10−3−10−6, 10−2−10−5, 10−4−10−5, 10−4−10−6, and 10−5−10−6, respectively. The results showed that mcr-1 plasmids can be easily transmitted to pathogenic bacteria by conjugation.

1. Introduction

The emergence of multidrug-resistant (MDR) pathogens, such as ESKAPE (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumonia, Acinetobacter baumannii, Pseudomonas aeruginosa, Enterobacter spp., or recently Enterobacteriaceae) and the lack of effective antimicrobials are a serious issue in public health [1]. Colistin is one of the last-resort antibiotics to treat MDR Gram-negative bacteria, and its binding to the lipid A moiety of lipopolysaccharide (LPS) destabilizes the outer membrane and results in cell death [2]. Colistin resistance is mainly associated with the modification of LPS, such as phosphoethanolamine modification of lipid A [3,4,5], and causes serous clinical problems in the control of Gram-negative pathogens in ESKAPE [6,7,8].
Since the first discovery of the mobilized colistin resistance (mcr)-1 gene on plasmids in Escherichia coli by Liu et al. in China, 2016 [4], E. coli strains harboring mcr-1 have been reported in many countries throughout America, Asia, and Europe [4,9,10] and have been isolated from various sources, such as animals, humans, environmental samples, and food [10,11,12]. In South Korea, mcr-1-positive E. coli strains have been isolated in livestock and humans [13,14]. However, there have been no studies about mcr-1-positive E. coli from retail food in the country.
Several recent reports also suggested that the spread of mcr-1 to multidrug-resistant bacteria can contribute to the development of the pan drug-resistant (PDR) phenotype, since mcr-1 on plasmids can be easily disseminated [3,15]. The increasing number of PDR bacteria, including E. coli, is considered a threat to public health [16]. E. coli is a major cause of human diseases, such as urinary tract infections, sepsis, and pneumonia [17]. Therefore, the emergence of PDR E. coli isolates, particularly those harboring extended-spectrum β-lactamase (ESBL) and plasmid-mediated quinolone resistance (PMQR) genes, have aggravated the public health burdens of antibiotic resistance.
A number of studies have shown that retail chicken is a major reservoir of disseminating antibiotic-resistant E. coli to humans [9,18,19]. In this study, we aimed at isolating mcr-1-positive E. coli strains from retail chicken in South Korea, characterizing the DNA sequence of the mcr-1 plasmids, and determining the frequencies of conjugational transfer of mcr-1 plasmids to other Gram-negative pathogens.

2. Materials and Methods

2.1. Bacterial Strains and Culture Methods

Three mcr-1-positive E. coli strains (JSMCR1, FORC81 and FORC82) were isolated from retail raw chicken in South Korea in our previous study [20]. The mcr-1-positive E. coli strains, E. coli ATCC 43889 (Enterohemorrhagic E. coli; EHEC), E. coli NCCP 14039 (Enteroaggregative E. coli; EAEC), enterotoxigenic E. coli (ETEC, a laboratory collection), Salmonella enetrica serovar Typhimurium SL1344, and K. pneumoniae (a laboratory collection) were cultured on Luria–Bertani (LB) media at 37 °C. The pathogenic E. coli strains (EHEC, ETEC, EAEC), Salmonella Typhimurium, and Klebsiella were used as recipient strains in the conjugation assay.

2.2. Antimicrobial Susceptibility Testing

Antimicrobial susceptibility testing was performed with a broth dilution method as described previously [21,22] with ten antibiotics, including ampicillin, cephalothin, tetracycline, chloramphenicol, ciprofloxacin, kanamycin, gentamicin, streptomycin, polymyxin B, and colistin. E. coli ATCC 25922 was used as the quality control strain.

2.3. Conjugation Assay

For the selection of transconjugants, we first obtained spontaneous mutants of streptomycin-resistant recipient strains by culturing them on LB media supplemented with streptomycin. Donor and recipient cells were prepared by transferring 1% inoculum from overnight cultures into fresh LB broth, followed by incubation at 37 °C for 4 h with constant shaking. E. coli was conjugated with recipient cells at a ratio of 1:1. Cells were pelleted by centrifugation, washed twice with 10 mM MgSO4, and resuspended in 50 µL of MgSO4. The mixture of donor and recipient cells were spread on LB agars supplemented with streptomycin (2 µg/mL) and colistin (4 µg/mL). Transconjugants were confirmed with PCR using mcr-1-specific primers [4] and the recipient strains. Conjugation frequencies were calculated as the number of transconjugants per recipient cell.

2.4. Whole-Genome Sequencing

Whole-genome sequencing and assembly were performed commercially at ChunLab Inc. (Seoul, South Korea). The whole genome of E. coli JSMCR1, FORC81 and FORC82 was sequenced using PacBio RS II (Pacific Biosciences, Menlo Park, CA, USA). The genome sequences were annotated using the online Rapid Annotation Subsequencing Technology (RAST) and CLC Main Workbench 3.6.1 (CLC bio, Aarhus, Denmark), and deposited in the GenBank database with accession numbers CP030152-CP030157 (JSMCR1), CP029057-CP029061 (FORC81), and CP026641-CP026644 (FORC82).

3. Results and Discussion

3.1. Whole-Genome Sequencing of mcr-1-Positive E. coli Strains

Three mcr-1-positive E. coli strains (JSMCR1, FORC81 and FORC82) were isolated from retail chicken in South Korea. The results of whole genome sequencing revealed that the three mcr-1-postive E. coli strains possessed multiple plasmids and some of the plasmids harbored a number of antibiotic resistance genes (Table 1 and Figure S1). The three mcr-1-harboring plasmids belonged to the IncI2 type and possessed the genetic elements for bacterial conjugation (Table 1). The three mcr-1-harboring plasmids were similar to pHNSHP45 (accession no. KP347127), the first mcr-1-harboring plasmid isolated in China; pJSMCR1_4 (96% query coverage, 100% max nucleotide identity), pFORC81_2 (89% query coverage, 99% max nucleotide identity), and pFORC82_3 (97% query coverage, 99% max nucleotide identity). Unlike pHNSHP45, however, insertion sequences were not found in the plasmids (Figure 1). The sequences of the mcr-1-harboring plasmids were similar to the IncI2-type mcr-1-harboring plasmids, which were isolated from livestock and humans in Korea [13,14]. This is also consistent with a previous extensive analysis revealing that IncI2 is predominant in mcr-1-harboring plasmids in Asia, whereas IncHI2 plasmids are predominant in Europe [23].

3.2. Antimicrobial Susceptibility Profiles and Other Resistance Genes

All of the mcr-1-positive E. coli strains were highly resistant to most of the tested antibiotics belonging to different classes (Table 2). In particular, E. coli JSMCR1 was resistant to all the antibiotics tested in this study. Based on the results of whole genome sequencing, all isolates carried a few plasmids with different replicon types and multiple other antibiotic resistance genes conferring resistance to several different antibiotic classes (Table 1 and Figure S1). Whole-genome sequencing discovered point mutations in gyrA and parC, which confer resistance to fluoroquinolones; however, other antibiotic resistance genes were not found in the chromosome of the three strains, suggesting that pan drug resistance is primarily mediated by resistance plasmids in the strains.

3.3. Conjugation Assay

The conjugation experiments were performed with pathogenic E. coli strains (EHEC, ETEC, EAEC), Salmonella Typhimurium, and Klebsiella as the recipient strains. The results of the antimicrobial susceptibility test showed that only the minimum inhibitory concentrations (MICs) of polymyxin B and colistin were increased in transconjugants from two-fold to 16-fold compared to their parental strains (Table 2). However, other plasmids harboring antibiotic resistance genes, which were simultaneously present in the mcr-1-postive strains, were not transferred to the recipient strains under the experimental settings based on PCR testing with primers specific to the plasmids. These results indicated that mcr-1 plasmids are highly transmissible compared to other resistance plasmids; this presumably enables mcr-1 plasmids to be disseminated from E. coli to Gram-negative bacteria [4,24].
To confirm this, we determined the conjugational frequency of mcr-1 plasmids and found that the transmission rates of the mcr-1 plasmids were 10−3–10−6 in EHEC, 10−2–10−5 in ETEC, 10−4–10−5 in EAEC, 10−4–10−6 in Salmonella, and 10−5–10−6 in Klebsiella (Figure 2). Conjugation frequencies varied depending on the recipient strain. For instance, the conjugation frequencies of pFORC81-2 were as high as 3 × 10−3 in ETEC and as low as 2 × 10−6 in EHEC (Figure 2). The frequencies of conjugational transfer of the mcr-1 plasmids to E. coli strains were similar to previous studies [25]. Furthermore, in this study, we demonstrated that mcr-1 plasmids were transmitted to other Gram-negative bacteria, such as Salmonella and Klebsiella, at the frequencies comparable to those observed in E. coli (Figure 2).

4. Conclusions

In this study, we isolated and characterized three mcr-1 plasmids from PDR E. coli strains from retail raw chicken in South Korea. Although the number of isolated plasmids was small, the findings of this study are important because this is the first report about mcr-1 plasmids originating from retail food in the country. The whole genome sequencing of the PDR E. coli strains showed that all the genetic determinants for antibiotic resistance were associated with plasmids, except for fluoroquinolone resistance caused by point mutations in gyrA and parC. The mcr-1 plasmids were highly transferrable to pathogenic E. coli strains, Salmonella, and Klebsiella. This may allow colistin resistance to easily spread in the food supply system.

Supplementary Materials

Supplementary materials can be found at Figure S1: Circular map of plasmid pJSMCR1_1 (A), pJSMCR1_2 (B), pFORC81_1 (C), and pFORC82_1 (D).

Author Contributions

S.R. and B.J. designed the study; J.K., B.K.H., and H.C. performed the experiments. J.K. and B.J. analyzed the data; J.K. and B.J. wrote the manuscript; J.K., Y.W., S.H.C., S.R., and B.J. critically reviewed the manuscript.


This research was funded by a grant (14162MFDS972, 19162MFDS037) from the Ministry of Food and Drug Safety in 2019. J.K. was supported by the BK21 Plus Program of Department of Agricultural Biotechnology, Seoul National University, Seoul, Korea.

Conflicts of Interest

The authors declare no conflict of interest.


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Figure 1. Sequence comparison of mcr-1-harboring plasmids. pHNSHP45 was used as a reference. Black inner ring indicated the pan-genome of the mcr-1-harboring plasmid.
Figure 1. Sequence comparison of mcr-1-harboring plasmids. pHNSHP45 was used as a reference. Black inner ring indicated the pan-genome of the mcr-1-harboring plasmid.
Microorganisms 07 00344 g001
Figure 2. Conjugation frequencies of three mcr-1 plasmids from E. coli isolates from retail chicken. The data represent the means and standard deviations of the results from three independent experiments.
Figure 2. Conjugation frequencies of three mcr-1 plasmids from E. coli isolates from retail chicken. The data represent the means and standard deviations of the results from three independent experiments.
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Table 1. Plasmids present in E. coli isolates harboring mcr-1.
Table 1. Plasmids present in E. coli isolates harboring mcr-1.
E. coli StrainPlasmidSize (bp)GenBank Accession No.Inc GroupResistance Genes
JSMCR1pJSMCR1_1152,677CP030153IncFIB, IncFIIaph(3′)-Ia, aac(3)-IId, blaCTX-M-65, fosA3
pJSMCR1_2134,064CP030154p0111aadA1, blaOXA-10, qnrS1, floR, cmlA1, arr-2, tet(A), dfrA14
FORC81pFORC81_1253,947CP029058IncI1, IncFIIaadA1, aadA2, aac(3)-IId, blaTEM-1B,
qnrS1, floR, cmlA1, sul3, tet(A), dfrA12
pFORC81_432,945CP029061IncI1blaTEM-1B, floR
FORC82pFORC82_1250,778CP026642IncHI2A, IncHI2, IncNaadA1, aph(3′’)-Ib, aph(6)-Id, blaCTX-M-65, blaOXA-10, qnrS1, mph(A), floR, cmlA1,
arr-2, sul2, tet(M), tet(A), dfrA14
pFORC82_2101,404CP026643IncFIC, IncFIB-
Table 2. Minimum inhibitory concentrations (MICs) of mcr-1-positive E. coli strains and their transconjugants.
Table 2. Minimum inhibitory concentrations (MICs) of mcr-1-positive E. coli strains and their transconjugants.
StrainOrigin amcr-1 Gene bMIC c (μg/mL)
E. coli JSMCR1WT+>64>64128>64>8>32>646488
E. coli FORC81WT+>6464>128>64>88>64888
E. coli FORC82WT+>64>6412864242288
EHEC (E. coli ATCC 43889)WT-≤0.5≤0.5≤0.0628≤0.5≤0.0039≤0.25≤0.5>128≤0.25≤0.25
ETEC (isolate)WT->64832640.0312>32>64>12842
EAEC (E. coli NCCP 14039)WT->6416>12840.031282>12842
S. Typhimurium SL1344WT-220.540.015642>12844
Klebsiella (isolate)WT->6416>128>64>16>321>12844
a WT: wild type, TC: Transconjugant. b Presence (+) or absence (-) of mcr-1, based on PCR and confirmed by sequencing. c AMP: ampicillin, CEF: cephalothin, TET: tetracycline, CHL: chloramphenicol, CIP: ciprofloxacin, KAN: Kanamycin; GEN: gentamicin; STR: streptomycin; POL: polymyxin B; COL: colistin.

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MDPI and ACS Style

Kim, J.; Hwang, B.K.; Choi, H.; Wang, Y.; Choi, S.H.; Ryu, S.; Jeon, B. Characterization of mcr-1-Harboring Plasmids from Pan Drug-Resistant Escherichia coli Strains Isolated from Retail Raw Chicken in South Korea. Microorganisms 2019, 7, 344.

AMA Style

Kim J, Hwang BK, Choi H, Wang Y, Choi SH, Ryu S, Jeon B. Characterization of mcr-1-Harboring Plasmids from Pan Drug-Resistant Escherichia coli Strains Isolated from Retail Raw Chicken in South Korea. Microorganisms. 2019; 7(9):344.

Chicago/Turabian Style

Kim, Jinshil, Bo Kyoung Hwang, HyeLim Choi, Yang Wang, Sang Ho Choi, Sangryeol Ryu, and Byeonghwa Jeon. 2019. "Characterization of mcr-1-Harboring Plasmids from Pan Drug-Resistant Escherichia coli Strains Isolated from Retail Raw Chicken in South Korea" Microorganisms 7, no. 9: 344.

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