Extended-spectrum β-lactamase-producing Escherichia coli isolated from captive primates: characteristics and horizontal gene transfer ability analysis.

The rapid spread of extended-spectrum β-lactamases (ESBLs)-producing Escherichia coli (ESBL-EC) around the world has become a significant challenge for humans and animals. In this study, we aimed to examine the characteristics and horizontal gene transfer (HGT) capacity of ESBL-EC derived from capti...

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Main Authors: Wenhao Zhong, Yuxin Zhou, Mengjie Che, Liqin Wang, Xingyu Tian, Chengdong Wang, Yuehong Cheng, Haifeng Liu, Ziyao Zhou, Guangneng Peng, Kun Zhang, Yan Luo, Keyun Shi, Zhijun Zhong
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0321514
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author Wenhao Zhong
Yuxin Zhou
Mengjie Che
Liqin Wang
Xingyu Tian
Chengdong Wang
Yuehong Cheng
Haifeng Liu
Ziyao Zhou
Guangneng Peng
Kun Zhang
Yan Luo
Keyun Shi
Zhijun Zhong
author_facet Wenhao Zhong
Yuxin Zhou
Mengjie Che
Liqin Wang
Xingyu Tian
Chengdong Wang
Yuehong Cheng
Haifeng Liu
Ziyao Zhou
Guangneng Peng
Kun Zhang
Yan Luo
Keyun Shi
Zhijun Zhong
author_sort Wenhao Zhong
collection DOAJ
description The rapid spread of extended-spectrum β-lactamases (ESBLs)-producing Escherichia coli (ESBL-EC) around the world has become a significant challenge for humans and animals. In this study, we aimed to examine the characteristics and horizontal gene transfer (HGT) capacity of ESBL-EC derived from captive primates. We screened for ESBL-EC among a total of 444 multidrug-resistant (MDR) E. coli strains isolated from 13 zoos in China using double-disk test. ESBL genes, mobile genetic elements (MGEs), and virulence-associated genes (VAGs) in ESBL-EC were detected through polymerase chain reaction (PCR). Furthermore, conjugation experiments were conducted to examine the HGT capacity of ESBL-EC, and the population structure (phylogenetic groups and MLST) was determined. Our results showed that a total of 69 (15.54%, 69/444) ESBL-EC strains were identified, and 5 variants of blaCTX and 3 variants of blaTEM were detected. The highest detection rate was blaCTX-M-55 (49.28%, 34/69), followed by blaCTX-M-15 (39.13%, 27/69). Ten MGEs were detected and the most prevalent was IS26 (78.26%, 54/69), followed by ISEcp1 (60.87%, 42/69). Eighteen combinations of MGEs were detected, in which ISEcp1 + IS26 was predominant (18.84%, n = 13). A total of 15 VAGs were detected and the most prevalent was fimC (84.06%, 58/69), followed by sitA (78.26%, 54/69). Furthermore, HGT ability analysis results showed that 40.58% (28/69) of ESBL-EC strains exhibited the ability to engage in conjugative transfer. Plasmid typing revealed that IncFIB (78.57%, 22/28) had the highest detection rates. Furthermore, antibiotic resistance genes (ARGs) of blaTEM-135, tetA and qnrS; MGEs of IS26, trbC and ISCR3/14 showed high rates of conjugative transfer. The population structure analysis showed that the phylogroup B1 and ST2161 were the most prevalent. ESBL-EC poses a potential threat to captive primates and may spread to other animals, humans, and the environment. It is imperative to implement measures to prevent the transmission of ESBL-EC among captive primates.
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spelling doaj-art-74e7a94ffe5a4b64a9491da8b65727462025-08-20T02:26:28ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01204e032151410.1371/journal.pone.0321514Extended-spectrum β-lactamase-producing Escherichia coli isolated from captive primates: characteristics and horizontal gene transfer ability analysis.Wenhao ZhongYuxin ZhouMengjie CheLiqin WangXingyu TianChengdong WangYuehong ChengHaifeng LiuZiyao ZhouGuangneng PengKun ZhangYan LuoKeyun ShiZhijun ZhongThe rapid spread of extended-spectrum β-lactamases (ESBLs)-producing Escherichia coli (ESBL-EC) around the world has become a significant challenge for humans and animals. In this study, we aimed to examine the characteristics and horizontal gene transfer (HGT) capacity of ESBL-EC derived from captive primates. We screened for ESBL-EC among a total of 444 multidrug-resistant (MDR) E. coli strains isolated from 13 zoos in China using double-disk test. ESBL genes, mobile genetic elements (MGEs), and virulence-associated genes (VAGs) in ESBL-EC were detected through polymerase chain reaction (PCR). Furthermore, conjugation experiments were conducted to examine the HGT capacity of ESBL-EC, and the population structure (phylogenetic groups and MLST) was determined. Our results showed that a total of 69 (15.54%, 69/444) ESBL-EC strains were identified, and 5 variants of blaCTX and 3 variants of blaTEM were detected. The highest detection rate was blaCTX-M-55 (49.28%, 34/69), followed by blaCTX-M-15 (39.13%, 27/69). Ten MGEs were detected and the most prevalent was IS26 (78.26%, 54/69), followed by ISEcp1 (60.87%, 42/69). Eighteen combinations of MGEs were detected, in which ISEcp1 + IS26 was predominant (18.84%, n = 13). A total of 15 VAGs were detected and the most prevalent was fimC (84.06%, 58/69), followed by sitA (78.26%, 54/69). Furthermore, HGT ability analysis results showed that 40.58% (28/69) of ESBL-EC strains exhibited the ability to engage in conjugative transfer. Plasmid typing revealed that IncFIB (78.57%, 22/28) had the highest detection rates. Furthermore, antibiotic resistance genes (ARGs) of blaTEM-135, tetA and qnrS; MGEs of IS26, trbC and ISCR3/14 showed high rates of conjugative transfer. The population structure analysis showed that the phylogroup B1 and ST2161 were the most prevalent. ESBL-EC poses a potential threat to captive primates and may spread to other animals, humans, and the environment. It is imperative to implement measures to prevent the transmission of ESBL-EC among captive primates.https://doi.org/10.1371/journal.pone.0321514
spellingShingle Wenhao Zhong
Yuxin Zhou
Mengjie Che
Liqin Wang
Xingyu Tian
Chengdong Wang
Yuehong Cheng
Haifeng Liu
Ziyao Zhou
Guangneng Peng
Kun Zhang
Yan Luo
Keyun Shi
Zhijun Zhong
Extended-spectrum β-lactamase-producing Escherichia coli isolated from captive primates: characteristics and horizontal gene transfer ability analysis.
PLoS ONE
title Extended-spectrum β-lactamase-producing Escherichia coli isolated from captive primates: characteristics and horizontal gene transfer ability analysis.
title_full Extended-spectrum β-lactamase-producing Escherichia coli isolated from captive primates: characteristics and horizontal gene transfer ability analysis.
title_fullStr Extended-spectrum β-lactamase-producing Escherichia coli isolated from captive primates: characteristics and horizontal gene transfer ability analysis.
title_full_unstemmed Extended-spectrum β-lactamase-producing Escherichia coli isolated from captive primates: characteristics and horizontal gene transfer ability analysis.
title_short Extended-spectrum β-lactamase-producing Escherichia coli isolated from captive primates: characteristics and horizontal gene transfer ability analysis.
title_sort extended spectrum β lactamase producing escherichia coli isolated from captive primates characteristics and horizontal gene transfer ability analysis
url https://doi.org/10.1371/journal.pone.0321514
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