Widespread prevalence and molecular epidemiology of tet(X4) and mcr-1 harboring Escherichia coli isolated from chickens in Pakistan
The emergence and spread of plasmid-mediated tigecycline resistance gene tet(X4) and colistin resistance gene mcr-1 in Escherichia coli (E. coli) pose a potential threat to public health, due to the importance of colistin and tigecycline for treating serious clinical infections. However, the charact...
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Published in: | The Science of the total environment Vol. 806; no. Pt 2; p. 150689 |
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Abstract | The emergence and spread of plasmid-mediated tigecycline resistance gene tet(X4) and colistin resistance gene mcr-1 in Escherichia coli (E. coli) pose a potential threat to public health, due to the importance of colistin and tigecycline for treating serious clinical infections. However, the characterization of bacteria coharboring both genes was few reported. Here, we described the molecular epidemiology of tet(X4) and mcr-1 harboring E. coli strains of chicken origin in Pakistan, with methods including PCR, antimicrobial susceptibility testing, DNA transfer assays, plasmid replicon typing, whole-genome sequencing and bioinformatics analysis. The tet(X4) gene was identified in 36 isolates exhibiting high levels of tigecycline resistance (MICs, 16–128 mg/L). Worryingly, 24 of the 36 tet(X4)-bearing isolates were confirmed as colistin resistance, positive for plasmid-borne mcr-1. We observed the prevalence of tet(X4)-bearing IncFII plasmid with mcr-1-bearing IncI2 plasmid in 12 E. coli isolates, with a high co-transfer frequency except for one strain PK8233, in which tet(X4)- and mcr-1-bearing plasmids were non-transferable. Coexistence of tet(X4)-bearing IncFII plasmid with mcr-1-carrying multidrug-resistant (MDR) IncHI2 plasmid was also identified in 10 E. coli isolates, and a relatively low co-transfer frequency was obtained except PK8575, in which mcr-1 was non-transferable. The transferability of pPK8275-tetX in PK8275 and pPK8233-tetX in PK8233, that could transfer from E. coli J53 to C600 by conjugation, was interfered by certain factors in PK8275 and PK8233. This may provide new insights to prevent and control the spread of antibiotic resistance genes. Two strains were reported to co-carry tet(X4)-positive IncQ1 plasmid and mcr-1-positive IncI2 plasmid. Convergence of tet(X4) and mcr-1 genes in E. coli by conjugative or mobilizable plasmids may lead to potentially widespread transmission of such resistance genes, which may incur antibiotic-resistance crisis globally.
[Display omitted]
•First comprehensive characterization of E. coli isolates co-carrying tet(X4) and mcr-1 outside of China•High co-transfer frequencies of tet(X4) and mcr-1 were observed.•The tet(X4) and mcr-1 harboring E. coli isolates were prevalent in food animals in Pakistan.•Plasmids were major contributors to transmission of the two vital resistance genes in different bacterial clones. |
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AbstractList | The emergence and spread of plasmid-mediated tigecycline resistance gene tet(X4) and colistin resistance gene mcr-1 in Escherichia coli (E. coli) pose a potential threat to public health, due to the importance of colistin and tigecycline for treating serious clinical infections. However, the characterization of bacteria coharboring both genes was few reported. Here, we described the molecular epidemiology of tet(X4) and mcr-1 harboring E. coli strains of chicken origin in Pakistan, with methods including PCR, antimicrobial susceptibility testing, DNA transfer assays, plasmid replicon typing, whole-genome sequencing and bioinformatics analysis. The tet(X4) gene was identified in 36 isolates exhibiting high levels of tigecycline resistance (MICs, 16-128 mg/L). Worryingly, 24 of the 36 tet(X4)-bearing isolates were confirmed as colistin resistance, positive for plasmid-borne mcr-1. We observed the prevalence of tet(X4)-bearing IncFII plasmid with mcr-1-bearing IncI2 plasmid in 12 E. coli isolates, with a high co-transfer frequency except for one strain PK8233, in which tet(X4)- and mcr-1-bearing plasmids were non-transferable. Coexistence of tet(X4)-bearing IncFII plasmid with mcr-1-carrying multidrug-resistant (MDR) IncHI2 plasmid was also identified in 10 E. coli isolates, and a relatively low co-transfer frequency was obtained except PK8575, in which mcr-1 was non-transferable. The transferability of pPK8275-tetX in PK8275 and pPK8233-tetX in PK8233, that could transfer from E. coli J53 to C600 by conjugation, was interfered by certain factors in PK8275 and PK8233. This may provide new insights to prevent and control the spread of antibiotic resistance genes. Two strains were reported to co-carry tet(X4)-positive IncQ1 plasmid and mcr-1-positive IncI2 plasmid. Convergence of tet(X4) and mcr-1 genes in E. coli by conjugative or mobilizable plasmids may lead to potentially widespread transmission of such resistance genes, which may incur antibiotic-resistance crisis globally. The emergence and spread of plasmid-mediated tigecycline resistance gene tet(X4) and colistin resistance gene mcr-1 in Escherichia coli (E. coli) pose a potential threat to public health, due to the importance of colistin and tigecycline for treating serious clinical infections. However, the characterization of bacteria coharboring both genes was few reported. Here, we described the molecular epidemiology of tet(X4) and mcr-1 harboring E. coli strains of chicken origin in Pakistan, with methods including PCR, antimicrobial susceptibility testing, DNA transfer assays, plasmid replicon typing, whole-genome sequencing and bioinformatics analysis. The tet(X4) gene was identified in 36 isolates exhibiting high levels of tigecycline resistance (MICs, 16–128 mg/L). Worryingly, 24 of the 36 tet(X4)-bearing isolates were confirmed as colistin resistance, positive for plasmid-borne mcr-1. We observed the prevalence of tet(X4)-bearing IncFII plasmid with mcr-1-bearing IncI2 plasmid in 12 E. coli isolates, with a high co-transfer frequency except for one strain PK8233, in which tet(X4)- and mcr-1-bearing plasmids were non-transferable. Coexistence of tet(X4)-bearing IncFII plasmid with mcr-1-carrying multidrug-resistant (MDR) IncHI2 plasmid was also identified in 10 E. coli isolates, and a relatively low co-transfer frequency was obtained except PK8575, in which mcr-1 was non-transferable. The transferability of pPK8275-tetX in PK8275 and pPK8233-tetX in PK8233, that could transfer from E. coli J53 to C600 by conjugation, was interfered by certain factors in PK8275 and PK8233. This may provide new insights to prevent and control the spread of antibiotic resistance genes. Two strains were reported to co-carry tet(X4)-positive IncQ1 plasmid and mcr-1-positive IncI2 plasmid. Convergence of tet(X4) and mcr-1 genes in E. coli by conjugative or mobilizable plasmids may lead to potentially widespread transmission of such resistance genes, which may incur antibiotic-resistance crisis globally. [Display omitted] •First comprehensive characterization of E. coli isolates co-carrying tet(X4) and mcr-1 outside of China•High co-transfer frequencies of tet(X4) and mcr-1 were observed.•The tet(X4) and mcr-1 harboring E. coli isolates were prevalent in food animals in Pakistan.•Plasmids were major contributors to transmission of the two vital resistance genes in different bacterial clones. |
ArticleNumber | 150689 |
Author | Li, Ruichao Mohsin, Mashkoor Munir, Asim Liu, Yuan Abdullah, Sabahat Lu, Xiaoyu Wang, Zhiqiang Xiao, Xia |
Author_xml | – sequence: 1 givenname: Ruichao surname: Li fullname: Li, Ruichao organization: Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu Province, PR China – sequence: 2 givenname: Xiaoyu surname: Lu fullname: Lu, Xiaoyu organization: Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu Province, PR China – sequence: 3 givenname: Asim surname: Munir fullname: Munir, Asim organization: Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan – sequence: 4 givenname: Sabahat surname: Abdullah fullname: Abdullah, Sabahat organization: Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan – sequence: 5 givenname: Yuan surname: Liu fullname: Liu, Yuan organization: Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu Province, PR China – sequence: 6 givenname: Xia surname: Xiao fullname: Xiao, Xia organization: Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu Province, PR China – sequence: 7 givenname: Zhiqiang surname: Wang fullname: Wang, Zhiqiang email: zqwang@yzu.edu.cn organization: Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu Province, PR China – sequence: 8 givenname: Mashkoor surname: Mohsin fullname: Mohsin, Mashkoor email: mashkoormohsin@uaf.edu.pk organization: Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan |
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CitedBy_id | crossref_primary_10_1016_j_fm_2022_104188 crossref_primary_10_3389_fmicb_2022_969769 crossref_primary_10_3390_pathogens12070903 crossref_primary_10_3389_fmicb_2022_808744 crossref_primary_10_3389_fcimb_2024_1399732 crossref_primary_10_1016_j_soh_2024_100069 crossref_primary_10_3390_antibiotics12030488 crossref_primary_10_1128_spectrum_00196_22 crossref_primary_10_1038_s41598_024_59201_5 crossref_primary_10_1016_S2666_5247_22_00387_1 crossref_primary_10_1128_spectrum_03639_22 crossref_primary_10_3389_fmicb_2022_852488 crossref_primary_10_1016_j_ijantimicag_2023_106961 crossref_primary_10_1016_j_micres_2024_127730 crossref_primary_10_1093_jacamr_dlad119 crossref_primary_10_1128_spectrum_03969_23 crossref_primary_10_3390_antibiotics12071117 crossref_primary_10_3390_ijms24086923 crossref_primary_10_3390_microorganisms10020394 crossref_primary_10_1007_s00253_024_13191_6 crossref_primary_10_1016_j_jgar_2024_04_001 |
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Keywords | Co-transfer frequency tet(X4) Coexistence Escherichia coli Chickens mcr-1 |
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SubjectTerms | Animals Chickens Co-transfer frequency Coexistence Escherichia coli Escherichia coli - genetics Escherichia coli Proteins - genetics mcr-1 Molecular Epidemiology Pakistan - epidemiology Prevalence tet(X4) |
Title | Widespread prevalence and molecular epidemiology of tet(X4) and mcr-1 harboring Escherichia coli isolated from chickens in Pakistan |
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