Amplification of the Chromosomal blaCTX-M-14 Gene in Escherichia coli Expanding the Spectrum of Resistance under Antimicrobial Pressure

ABSTRACT Various forms of adaptive evolution occur in clinical isolates in response to the presence of antimicrobial drugs. Among a total of 171 CTX-M-9 group/family extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli blood isolates recovered between 2016 and 2017 in six general hospi...

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Main Authors: Eun-Jeong Yoon, You Jeong Choi, Dokyun Kim, Dongju Won, Jong Rak Choi, Seok Hoon Jeong
Format: Article
Language:English
Published: American Society for Microbiology 2022-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.00319-22
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author Eun-Jeong Yoon
You Jeong Choi
Dokyun Kim
Dongju Won
Jong Rak Choi
Seok Hoon Jeong
author_facet Eun-Jeong Yoon
You Jeong Choi
Dokyun Kim
Dongju Won
Jong Rak Choi
Seok Hoon Jeong
author_sort Eun-Jeong Yoon
collection DOAJ
description ABSTRACT Various forms of adaptive evolution occur in clinical isolates in response to the presence of antimicrobial drugs. Among a total of 171 CTX-M-9 group/family extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli blood isolates recovered between 2016 and 2017 in six general hospitals, 50.3% of the isolates possessed the blaCTX-M-14-like gene in their chromosome rather than in a plasmid. Focusing on this unprecedented way of the blaCTX-M ESBL gene possession, molecular epidemiology of the isolates was assessed and the chromosomal location of the acquired cephalosporinase gene was dissected in an evolutionary point of view. Taking advantage of a complete collection of E. coli blood isolates from a limited period, clonal relatedness of the E. coli isolates carrying the blaCTX-M-14-like gene was clarified and the dominant clone, ST131 H30R, was identified. To control the level of resistance and the resistance spectrum to oxyimino-cephalosporin drugs, transcription level of the blaCTX-M-14-like gene was tuned finely through positioning the gene near the chromosomal initiation dnaA gene and amplifying numbers of the gene in a chromosome using either the copy-and-paste or the tandem amplification methods. Inconspicuous fitness cost by chromosomal location of the gene and free adjustment of the oxyimino-cephalosporin resistance would urge the dominancy of E. coli clinical isolates harboring the blaCTX-M ESBL gene in their chromosome. IMPORTANCE Increasing prevalence of E. coli producing CTX-M ESBL is a major concern in clinical settings because it significantly limits treatment options. Thus, it is important to keep watching current molecular mechanisms of resistance and the scheme for dissemination. Recently, chromosomal locations of the blaCTX-M genes are often documented in clinical settings and the bacterial strategies were needed to be dissected in an evolutionary point of view. Both main mechanisms of fine tuning the chromosomal gene expression, bacterial gene amplification either by copy-and-paste or by tandem amplification and positioning the gene near the chromosomal initiation dnaA gene, were demonstrated in the study, and the fitness cost by the chromosomal location was evaluated.
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spelling doaj.art-218b5bd790274d1683a487d708cce6992022-12-22T02:39:00ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.00319-22Amplification of the Chromosomal blaCTX-M-14 Gene in Escherichia coli Expanding the Spectrum of Resistance under Antimicrobial PressureEun-Jeong Yoon0You Jeong Choi1Dokyun Kim2Dongju Won3Jong Rak Choi4Seok Hoon Jeong5Department of Laboratory Medicine, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine, Yonsei University College of Medicine, Seoul, South KoreaDepartment of Laboratory Medicine, Yonsei University College of Medicine, Seoul, South KoreaABSTRACT Various forms of adaptive evolution occur in clinical isolates in response to the presence of antimicrobial drugs. Among a total of 171 CTX-M-9 group/family extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli blood isolates recovered between 2016 and 2017 in six general hospitals, 50.3% of the isolates possessed the blaCTX-M-14-like gene in their chromosome rather than in a plasmid. Focusing on this unprecedented way of the blaCTX-M ESBL gene possession, molecular epidemiology of the isolates was assessed and the chromosomal location of the acquired cephalosporinase gene was dissected in an evolutionary point of view. Taking advantage of a complete collection of E. coli blood isolates from a limited period, clonal relatedness of the E. coli isolates carrying the blaCTX-M-14-like gene was clarified and the dominant clone, ST131 H30R, was identified. To control the level of resistance and the resistance spectrum to oxyimino-cephalosporin drugs, transcription level of the blaCTX-M-14-like gene was tuned finely through positioning the gene near the chromosomal initiation dnaA gene and amplifying numbers of the gene in a chromosome using either the copy-and-paste or the tandem amplification methods. Inconspicuous fitness cost by chromosomal location of the gene and free adjustment of the oxyimino-cephalosporin resistance would urge the dominancy of E. coli clinical isolates harboring the blaCTX-M ESBL gene in their chromosome. IMPORTANCE Increasing prevalence of E. coli producing CTX-M ESBL is a major concern in clinical settings because it significantly limits treatment options. Thus, it is important to keep watching current molecular mechanisms of resistance and the scheme for dissemination. Recently, chromosomal locations of the blaCTX-M genes are often documented in clinical settings and the bacterial strategies were needed to be dissected in an evolutionary point of view. Both main mechanisms of fine tuning the chromosomal gene expression, bacterial gene amplification either by copy-and-paste or by tandem amplification and positioning the gene near the chromosomal initiation dnaA gene, were demonstrated in the study, and the fitness cost by the chromosomal location was evaluated.https://journals.asm.org/doi/10.1128/spectrum.00319-22CTX-M ESBLEscherichia coligene amplificationtranscription levelresistance spectrum
spellingShingle Eun-Jeong Yoon
You Jeong Choi
Dokyun Kim
Dongju Won
Jong Rak Choi
Seok Hoon Jeong
Amplification of the Chromosomal blaCTX-M-14 Gene in Escherichia coli Expanding the Spectrum of Resistance under Antimicrobial Pressure
Microbiology Spectrum
CTX-M ESBL
Escherichia coli
gene amplification
transcription level
resistance spectrum
title Amplification of the Chromosomal blaCTX-M-14 Gene in Escherichia coli Expanding the Spectrum of Resistance under Antimicrobial Pressure
title_full Amplification of the Chromosomal blaCTX-M-14 Gene in Escherichia coli Expanding the Spectrum of Resistance under Antimicrobial Pressure
title_fullStr Amplification of the Chromosomal blaCTX-M-14 Gene in Escherichia coli Expanding the Spectrum of Resistance under Antimicrobial Pressure
title_full_unstemmed Amplification of the Chromosomal blaCTX-M-14 Gene in Escherichia coli Expanding the Spectrum of Resistance under Antimicrobial Pressure
title_short Amplification of the Chromosomal blaCTX-M-14 Gene in Escherichia coli Expanding the Spectrum of Resistance under Antimicrobial Pressure
title_sort amplification of the chromosomal blactx m 14 gene in escherichia coli expanding the spectrum of resistance under antimicrobial pressure
topic CTX-M ESBL
Escherichia coli
gene amplification
transcription level
resistance spectrum
url https://journals.asm.org/doi/10.1128/spectrum.00319-22
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