Characterization of a blaCTX-M-3, blaKPC-2 and blaTEM-1B co-producing IncN plasmid in Escherichia coli of chicken origin
WANG Wen-jing1, 2*, WANG Yi-fu1, 2*, JIN Ya-jie2, SONG Wu-qiang2, LIN Jia-meng2, ZHANG Yan2, TONG Xin-ru2, TU Jian1, 3, LI Rui-chao4, LI Tao2
1 Hunan Provincial Key Laboratory of Tumor Microenvironment Responsive Drug Research, Institute of Pharmacy and Pharmacology, University of South China, Hengyang 421001, P.R.China
2 Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, P.R.China
3 Guilin Medical University, Guilin 541199, P.R.China
4 Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, P.R.China
An extensively drug-resistant (XDR) Escherichia coli strain 258E was isolated from an anal swab sample of a chicken farm of Anhui province in China. Genomic analyses indicated that the strain 258E harbors an incompatibility group N (IncN) plasmid pEC258-3, which co-produces blaCTX-M-3, blaKPC-2, blaTEM-1B, qnrS1, aac(6')-Ib-cr, dfrA14, arr-3, and aac(6')-Ib3. Multiple genome arrangement analyses indicated that pEC258-3 is highly homologous with pCRKP-1-KPC discovered in Klebsiella pneumoniae from a patient. Furthermore, conjugation experiments proved that plasmid pEC258-3 can be transferred horizontally and may pose a significant potential threat in animals, community and hospital settings.
The work was funded by the National Key Research and Development Program of China (2018YFE0192600), the Shanghai Agriculture Applied Technology Development Program, China (T20200104), the Fundamental Research Funds for the Central Universities, China (2020JB05), and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (CAAS-ZDRW202203).
About author: WANG Wen-jing, E-mail: 2810716541@qq.com; Correspondence LI Tao, Tel: +86-21-34293156, E-mail: litao@shvri.ac.cn; TU Jian, E-mail: 2001001806@usc.edu.cn; LI Rui-chao, E-mail: rchl88@yzu.edu.cn
* These authors contributed equally to this study.
WANG Wen-jing, WANG Yi-fu, JIN Ya-jie, SONG Wu-qiang, LIN Jia-meng, ZHANG Yan, TONG Xin-ru, TU Jian, LI Rui-chao, LI Tao.
2023.
Characterization of a blaCTX-M-3, blaKPC-2 and blaTEM-1B co-producing IncN plasmid in Escherichia coli of chicken origin
. Journal of Integrative Agriculture, 22(1): 320-324.
Bonardi S, Pitino R. 2019. Carbapenemase-producing bacteria in food-producing animals, wildlife and environment: A challenge for human health. Italian Journal of Food Safety, 8, 7956.
Carattoli A. 2009. Resistance plasmid families in Enterobacteriaceae. Antimicrobial Agents and Chemotherapy, 53, 2227–2238.
Chen L, Hu H, Chavda K D, Zhao S, Liu R, Liang H, Zhang W, Wang X, Jacobs M R, Bonomo R A, Kreiswirth B N. 2014. Complete sequence of a KPC-producing IncN multidrug-resistant plasmid from an epidemic Escherichia coli sequence type 131 strain in China. Antimicrobial Agents and Chemotherapy, 58, 2422–2425.
Citterio B, Andreoni F, Simoni S, Carloni E, Magnani M, Mangiaterra G, Cedraro N, Biavasco F, Vignaroli C. 2020. Plasmid replicon typing of antibiotic-resistant Escherichia coli from clams and marine sediments. Frontiers in Microbiology, 11, 1101.
David S, Reuter S, Harris S R, Glasner C, Feltwell T, Argimon S, Abudahab K, Goater R, Giani T, Errico G, Aspbury M, Sjunnebo S, Eu S W G, Group E S, Feil E J, Rossolini G M, Aanensen D M, Grundmann H. 2019. Epidemic of carbapenem-resistant Klebsiella pneumoniae in Europe is driven by nosocomial spread. Nature Microbiology, 4, 1919–1929.
Day M J, Hopkins K L, Wareham D W, Toleman M A, Elviss N, Randall L, Teale C, Cleary P, Wiuff C, Doumith M, Ellington M J, Woodford N, Livermore D M. 2019. Extended-spectrum beta-lactamase-producing Escherichia coli in human-derived and foodchain-derived samples from England, Wales, and Scotland: An epidemiological surveillance and typing study. The Lancet Infectious Diseases, 19, 1325–1335.
Eikmeyer F, Hadiati A, Szczepanowski R, Wibberg D, Schneiker-Bekel S, Rogers L M, Brown C J, Top E M, Puhler A, Schluter A. 2012. The complete genome sequences of four new IncN plasmids from wastewater treatment plant effluent provide new insights into IncN plasmid diversity and evolution. Plasmid, 68, 13–24.
Golebiewski M, Kern-Zdanowicz I, Zienkiewicz M, Adamczyk M, Zylinska J, Baraniak A, Gniadkowski M, Bardowski J, Ceglowski P. 2007. Complete nucleotide sequence of the pCTX-M3 plasmid and its involvement in spread of the extended-spectrum beta-lactamase gene blaCTX-M–3. Antimicrobial Agents and Chemotherapy, 51, 3789–3795.
Grundmann H, Glasner C, Albiger B, Aanensen D M, Tomlinson C T, Andrasevic A T, Canton R, Carmeli Y, Friedrich A W, Giske C G, Glupczynski Y, Gniadkowski M, Livermore D M, Nordmann P, Poirel L, Rossolini G M, Seifert H, Vatopoulos A, Walsh T, Woodford N, et al. 2017. Occurrence of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli in the European survey of carbapenemase-producing Enterobacteriaceae (EuSCAPE): A prospective, multinational study. The Lancet Infectious Diseases, 17, 153–163.
Karabay O, Altindis M, Koroglu M, Karatuna O, Aydemir O A, Erdem A F. 2016. The carbapenem-resistant Enterobacteriaceae threat is growing: NDM-1 epidemic at a training hospital in Turkey. Annals of Clinical Microbiology and Antimicrobials, 15, 6.
Papp-Wallace K M, Endimiani A, Taracila M A, Bonomo R A. 2011. Carbapenems: Past, present, and future. Antimicrobial Agents & Chemotherapy, 55, 4943–4960.
Partridge S R, Kwong S M, Firth N, Jensen S O. 2018. Mobile genetic elements associated with antimicrobial resistance. Clinical Microbiology Reviews, 31, e00088–e00105.
Tilman D, Cassman K G, Matson P A, Naylor R, Polasky S. 2002. Agricultural sustainability and intensive production practices. Nature, 418, 671–677.
Zhang R, Liu L, Zhou H, Chan E W, Li J, Fang Y, Li Y, Liao K, Chen S. 2017. Nationwide surveillance of clinical carbapenem-resistant enterobacteriaceae (CRE) strains in China. EBioMedicine, 19, 98–106.