Characterization of a Novel Chromosomal Class C β-Lactamase, YOC-1, and Comparative Genomics Analysis of a Multidrug Resistance Plasmid in Yokenella regensburgei W13

Yokenella regensburgei, a member of the family Enterobacteriaceae, is usually isolated from environmental samples and generally resistant to early generations of cephalosporins. To characterize the resistance mechanism of Y. regensburgei strain W13 isolated from the sewage of an animal farm, whole g...

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Main Authors: Danying Zhou, Zhewei Sun, Junwan Lu, Hongmao Liu, Wei Lu, Hailong Lin, Xueya Zhang, Qiaoling Li, Wangxiao Zhou, Xinyi Zhu, Haili Xu, Xi Lin, Hailin Zhang, Teng Xu, Kewei Li, Qiyu Bao
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-08-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.02021/full
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author Danying Zhou
Danying Zhou
Danying Zhou
Zhewei Sun
Zhewei Sun
Junwan Lu
Junwan Lu
Hongmao Liu
Hongmao Liu
Wei Lu
Wei Lu
Hailong Lin
Hailong Lin
Hailong Lin
Xueya Zhang
Xueya Zhang
Xueya Zhang
Qiaoling Li
Qiaoling Li
Qiaoling Li
Wangxiao Zhou
Wangxiao Zhou
Xinyi Zhu
Xinyi Zhu
Haili Xu
Xi Lin
Xi Lin
Hailin Zhang
Hailin Zhang
Teng Xu
Kewei Li
Kewei Li
Qiyu Bao
Qiyu Bao
Qiyu Bao
author_facet Danying Zhou
Danying Zhou
Danying Zhou
Zhewei Sun
Zhewei Sun
Junwan Lu
Junwan Lu
Hongmao Liu
Hongmao Liu
Wei Lu
Wei Lu
Hailong Lin
Hailong Lin
Hailong Lin
Xueya Zhang
Xueya Zhang
Xueya Zhang
Qiaoling Li
Qiaoling Li
Qiaoling Li
Wangxiao Zhou
Wangxiao Zhou
Xinyi Zhu
Xinyi Zhu
Haili Xu
Xi Lin
Xi Lin
Hailin Zhang
Hailin Zhang
Teng Xu
Kewei Li
Kewei Li
Qiyu Bao
Qiyu Bao
Qiyu Bao
author_sort Danying Zhou
collection DOAJ
description Yokenella regensburgei, a member of the family Enterobacteriaceae, is usually isolated from environmental samples and generally resistant to early generations of cephalosporins. To characterize the resistance mechanism of Y. regensburgei strain W13 isolated from the sewage of an animal farm, whole genome sequencing, comparative genomics analysis and molecular cloning were performed. The results showed that a novel chromosomally encoded class C β-lactamase gene with the ability to confer resistance to β-lactam antibiotics, designated blaYOC–1, was identified in the genome of Y. regensburgei W13. Kinetic analysis revealed that the β-lactamase YOC-1 has a broad spectrum of substrates, including penicillins, cefazolin, cefoxitin and cefotaxime. The two functionally characterized β-lactamases with the highest amino acid identities to YOC-1 were CDA-1 (71.69%) and CMY-2 (70.65%). The genetic context of the blaYOC–1-ampR-encoding region was unique compared with the sequences in the NCBI nucleotide database. The plasmid pRYW13-125 of Y. regensburgei W13 harbored 11 resistance genes (blaOXA–10, blaLAP–2, dfrA14, tetA, tetR, cmlA5, floR, sul2, ant(3″)-IIa, arr-2 and qnrS1) within an ∼34 kb multidrug resistance region; these genes were all related to mobile genetic elements. The multidrug resistance region of pYRW13-125 shared the highest identities with those of two plasmids from clinical Klebsiella pneumoniae isolates, indicating the possibility of horizontal transfer of these resistance genes between bacteria of various origins.
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spelling doaj.art-bf37ad1db6ac4ed6aeb9ca515d092be72022-12-22T01:06:33ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-08-011110.3389/fmicb.2020.02021551059Characterization of a Novel Chromosomal Class C β-Lactamase, YOC-1, and Comparative Genomics Analysis of a Multidrug Resistance Plasmid in Yokenella regensburgei W13Danying Zhou0Danying Zhou1Danying Zhou2Zhewei Sun3Zhewei Sun4Junwan Lu5Junwan Lu6Hongmao Liu7Hongmao Liu8Wei Lu9Wei Lu10Hailong Lin11Hailong Lin12Hailong Lin13Xueya Zhang14Xueya Zhang15Xueya Zhang16Qiaoling Li17Qiaoling Li18Qiaoling Li19Wangxiao Zhou20Wangxiao Zhou21Xinyi Zhu22Xinyi Zhu23Haili Xu24Xi Lin25Xi Lin26Hailin Zhang27Hailin Zhang28Teng Xu29Kewei Li30Kewei Li31Qiyu Bao32Qiyu Bao33Qiyu Bao34The Second Affiliated Hospital and Yuying Children’s Hospital, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaThe Second Affiliated Hospital and Yuying Children’s Hospital, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaThe Second Affiliated Hospital and Yuying Children’s Hospital, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaThe Second Affiliated Hospital and Yuying Children’s Hospital, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaThe Second Affiliated Hospital and Yuying Children’s Hospital, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaThe Second Affiliated Hospital and Yuying Children’s Hospital, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaThe Second Affiliated Hospital and Yuying Children’s Hospital, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaThe Second Affiliated Hospital and Yuying Children’s Hospital, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaInstitute of Translational Medicine, Baotou Central Hospital, Baotou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaThe Second Affiliated Hospital and Yuying Children’s Hospital, Wenzhou Medical University, Wenzhou, ChinaKey Laboratory of Medical Genetics of Zhejiang Province, Key Laboratory of Laboratory Medicine, Ministry of Education of China, School of Laboratory Medicine and Life Sciences, Wenzhou Medical University, Wenzhou, ChinaInstitute of Biomedical Informatics, Wenzhou Medical University, Wenzhou, ChinaYokenella regensburgei, a member of the family Enterobacteriaceae, is usually isolated from environmental samples and generally resistant to early generations of cephalosporins. To characterize the resistance mechanism of Y. regensburgei strain W13 isolated from the sewage of an animal farm, whole genome sequencing, comparative genomics analysis and molecular cloning were performed. The results showed that a novel chromosomally encoded class C β-lactamase gene with the ability to confer resistance to β-lactam antibiotics, designated blaYOC–1, was identified in the genome of Y. regensburgei W13. Kinetic analysis revealed that the β-lactamase YOC-1 has a broad spectrum of substrates, including penicillins, cefazolin, cefoxitin and cefotaxime. The two functionally characterized β-lactamases with the highest amino acid identities to YOC-1 were CDA-1 (71.69%) and CMY-2 (70.65%). The genetic context of the blaYOC–1-ampR-encoding region was unique compared with the sequences in the NCBI nucleotide database. The plasmid pRYW13-125 of Y. regensburgei W13 harbored 11 resistance genes (blaOXA–10, blaLAP–2, dfrA14, tetA, tetR, cmlA5, floR, sul2, ant(3″)-IIa, arr-2 and qnrS1) within an ∼34 kb multidrug resistance region; these genes were all related to mobile genetic elements. The multidrug resistance region of pYRW13-125 shared the highest identities with those of two plasmids from clinical Klebsiella pneumoniae isolates, indicating the possibility of horizontal transfer of these resistance genes between bacteria of various origins.https://www.frontiersin.org/article/10.3389/fmicb.2020.02021/fullYokenella regensburgeiβ-lactamaseblaYOC–1kinetic analysisplasmid
spellingShingle Danying Zhou
Danying Zhou
Danying Zhou
Zhewei Sun
Zhewei Sun
Junwan Lu
Junwan Lu
Hongmao Liu
Hongmao Liu
Wei Lu
Wei Lu
Hailong Lin
Hailong Lin
Hailong Lin
Xueya Zhang
Xueya Zhang
Xueya Zhang
Qiaoling Li
Qiaoling Li
Qiaoling Li
Wangxiao Zhou
Wangxiao Zhou
Xinyi Zhu
Xinyi Zhu
Haili Xu
Xi Lin
Xi Lin
Hailin Zhang
Hailin Zhang
Teng Xu
Kewei Li
Kewei Li
Qiyu Bao
Qiyu Bao
Qiyu Bao
Characterization of a Novel Chromosomal Class C β-Lactamase, YOC-1, and Comparative Genomics Analysis of a Multidrug Resistance Plasmid in Yokenella regensburgei W13
Frontiers in Microbiology
Yokenella regensburgei
β-lactamase
blaYOC–1
kinetic analysis
plasmid
title Characterization of a Novel Chromosomal Class C β-Lactamase, YOC-1, and Comparative Genomics Analysis of a Multidrug Resistance Plasmid in Yokenella regensburgei W13
title_full Characterization of a Novel Chromosomal Class C β-Lactamase, YOC-1, and Comparative Genomics Analysis of a Multidrug Resistance Plasmid in Yokenella regensburgei W13
title_fullStr Characterization of a Novel Chromosomal Class C β-Lactamase, YOC-1, and Comparative Genomics Analysis of a Multidrug Resistance Plasmid in Yokenella regensburgei W13
title_full_unstemmed Characterization of a Novel Chromosomal Class C β-Lactamase, YOC-1, and Comparative Genomics Analysis of a Multidrug Resistance Plasmid in Yokenella regensburgei W13
title_short Characterization of a Novel Chromosomal Class C β-Lactamase, YOC-1, and Comparative Genomics Analysis of a Multidrug Resistance Plasmid in Yokenella regensburgei W13
title_sort characterization of a novel chromosomal class c β lactamase yoc 1 and comparative genomics analysis of a multidrug resistance plasmid in yokenella regensburgei w13
topic Yokenella regensburgei
β-lactamase
blaYOC–1
kinetic analysis
plasmid
url https://www.frontiersin.org/article/10.3389/fmicb.2020.02021/full
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