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Genome characteristics of the optrA-positive Clostridium perfringens strain QHY-2 carrying a novel plasmid type

Clostridium perfringens is a bacterial species of importance to both public and animal health. The gene optrA is the first gene that confers resistance to the tedizolid, a last-resort antimicrobial agent in human medicine. Herein, we whole-genome sequenced and analyzed one optrA-positive C. perfring...

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Autores principales: Wu, Ke, Li, Zhe, Fang, Mingjin, Yuan, Yuan, Fox, Edward M., Liu, Yingqiu, Li, Ruichao, Bai, Li, Zhang, Wen, Zhang, Wei-Min, Yang, Qi, Chang, Lingling, Li, Pu, Wang, Xinglong, Wang, Juan, Yang, Zengqi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469678/
https://www.ncbi.nlm.nih.gov/pubmed/37458450
http://dx.doi.org/10.1128/msystems.00535-23
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author Wu, Ke
Li, Zhe
Fang, Mingjin
Yuan, Yuan
Fox, Edward M.
Liu, Yingqiu
Li, Ruichao
Bai, Li
Zhang, Wen
Zhang, Wei-Min
Yang, Qi
Chang, Lingling
Li, Pu
Wang, Xinglong
Wang, Juan
Yang, Zengqi
author_facet Wu, Ke
Li, Zhe
Fang, Mingjin
Yuan, Yuan
Fox, Edward M.
Liu, Yingqiu
Li, Ruichao
Bai, Li
Zhang, Wen
Zhang, Wei-Min
Yang, Qi
Chang, Lingling
Li, Pu
Wang, Xinglong
Wang, Juan
Yang, Zengqi
author_sort Wu, Ke
collection PubMed
description Clostridium perfringens is a bacterial species of importance to both public and animal health. The gene optrA is the first gene that confers resistance to the tedizolid, a last-resort antimicrobial agent in human medicine. Herein, we whole-genome sequenced and analyzed one optrA-positive C. perfringens strain QHY-2 from Tibetan sheep in Qinghai province and identified one optrA plasmid pQHY-2. The plasmid shared similar structure with the optrA-positive plasmids p2C45 and p21-D-5b previously identified in C. perfringens, demonstrating the potential horizontal transmission of the optrA plasmids among C. perfringens strains. Annotation of the optrA-positive plasmids showed optrA and erm(A) located on a segment flanked by IS element IS1216E, and fexA, optrA, and erm(A) located on a segment flanked by IS element ISVlu1, which revealed the possible dissemination mechanism. Additionally, a Tn6218-like transposon carrying aac(6′)-aph(2″) and erm(B) was also detected on pQHY-2, demonstrating the transposition of Tn6218 and spread of antibiotic resistance among Clostridium bacteria. Molecular analysis indicated the optrA-positive plasmids belonged to a plasmid type distinct from the pCW3-like plasmids, pCP13-like plasmids, or pIP404-like plasmids. Further structure analysis showed they might be formed by inserting segments into plasmid pCPCPI53k-r1_1, which coexist with two pCW3-like plasmids and one pCP13-like plasmid in C. perfringens strain CPI 53k-r1 isolated from a healthy human in Finland. IMPORTANCE: Antimicrobial resistance is now a global concern posing threats to food safety and public health. The pCW3-like plasmids can encode several main toxin genes and three antibiotic resistance genes (ARGs), including tetA(P), tetB(P), and erm(B), which used to be considered as the main carrier of ARGs in Clostridium perfringens. In this study, we found the optrA plasmids, which belonged to a novel plasmid type, could also harbor many other ARGs, indicating this type of plasmid might be the potential repository of ARGs in C. perfringens. Additionally, this type of plasmid could coexist with the pCW3-like plasmids and pCP13-like plasmids that encoded toxin genes associated with gastrointestinal diseases, which showed the potential threat to public health.
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spelling pubmed-104696782023-09-01 Genome characteristics of the optrA-positive Clostridium perfringens strain QHY-2 carrying a novel plasmid type Wu, Ke Li, Zhe Fang, Mingjin Yuan, Yuan Fox, Edward M. Liu, Yingqiu Li, Ruichao Bai, Li Zhang, Wen Zhang, Wei-Min Yang, Qi Chang, Lingling Li, Pu Wang, Xinglong Wang, Juan Yang, Zengqi mSystems Research Article Clostridium perfringens is a bacterial species of importance to both public and animal health. The gene optrA is the first gene that confers resistance to the tedizolid, a last-resort antimicrobial agent in human medicine. Herein, we whole-genome sequenced and analyzed one optrA-positive C. perfringens strain QHY-2 from Tibetan sheep in Qinghai province and identified one optrA plasmid pQHY-2. The plasmid shared similar structure with the optrA-positive plasmids p2C45 and p21-D-5b previously identified in C. perfringens, demonstrating the potential horizontal transmission of the optrA plasmids among C. perfringens strains. Annotation of the optrA-positive plasmids showed optrA and erm(A) located on a segment flanked by IS element IS1216E, and fexA, optrA, and erm(A) located on a segment flanked by IS element ISVlu1, which revealed the possible dissemination mechanism. Additionally, a Tn6218-like transposon carrying aac(6′)-aph(2″) and erm(B) was also detected on pQHY-2, demonstrating the transposition of Tn6218 and spread of antibiotic resistance among Clostridium bacteria. Molecular analysis indicated the optrA-positive plasmids belonged to a plasmid type distinct from the pCW3-like plasmids, pCP13-like plasmids, or pIP404-like plasmids. Further structure analysis showed they might be formed by inserting segments into plasmid pCPCPI53k-r1_1, which coexist with two pCW3-like plasmids and one pCP13-like plasmid in C. perfringens strain CPI 53k-r1 isolated from a healthy human in Finland. IMPORTANCE: Antimicrobial resistance is now a global concern posing threats to food safety and public health. The pCW3-like plasmids can encode several main toxin genes and three antibiotic resistance genes (ARGs), including tetA(P), tetB(P), and erm(B), which used to be considered as the main carrier of ARGs in Clostridium perfringens. In this study, we found the optrA plasmids, which belonged to a novel plasmid type, could also harbor many other ARGs, indicating this type of plasmid might be the potential repository of ARGs in C. perfringens. Additionally, this type of plasmid could coexist with the pCW3-like plasmids and pCP13-like plasmids that encoded toxin genes associated with gastrointestinal diseases, which showed the potential threat to public health. American Society for Microbiology 2023-07-17 /pmc/articles/PMC10469678/ /pubmed/37458450 http://dx.doi.org/10.1128/msystems.00535-23 Text en Copyright © 2023 Wu et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Wu, Ke
Li, Zhe
Fang, Mingjin
Yuan, Yuan
Fox, Edward M.
Liu, Yingqiu
Li, Ruichao
Bai, Li
Zhang, Wen
Zhang, Wei-Min
Yang, Qi
Chang, Lingling
Li, Pu
Wang, Xinglong
Wang, Juan
Yang, Zengqi
Genome characteristics of the optrA-positive Clostridium perfringens strain QHY-2 carrying a novel plasmid type
title Genome characteristics of the optrA-positive Clostridium perfringens strain QHY-2 carrying a novel plasmid type
title_full Genome characteristics of the optrA-positive Clostridium perfringens strain QHY-2 carrying a novel plasmid type
title_fullStr Genome characteristics of the optrA-positive Clostridium perfringens strain QHY-2 carrying a novel plasmid type
title_full_unstemmed Genome characteristics of the optrA-positive Clostridium perfringens strain QHY-2 carrying a novel plasmid type
title_short Genome characteristics of the optrA-positive Clostridium perfringens strain QHY-2 carrying a novel plasmid type
title_sort genome characteristics of the optra-positive clostridium perfringens strain qhy-2 carrying a novel plasmid type
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469678/
https://www.ncbi.nlm.nih.gov/pubmed/37458450
http://dx.doi.org/10.1128/msystems.00535-23
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