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Integrative conjugative elements mediate the high prevalence of tmexCD3-toprJ1b in Proteus spp. of animal source

Integrative conjugative elements (ICEs) are important mobile elements that are associated with the dissemination of antibiotic resistance genes (ARGs) in Proteus. Recent studies demonstrated that the tigecycline resistance gene cluster tmexCD-toprJ has emerged in ICEs of Proteus. However, the preval...

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Autores principales: Peng, Kai, Li, Yangfan, Wang, Qiaojun, Yang, Pengbin, Wang, Zhiqiang, Li, Ruichao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10654056/
https://www.ncbi.nlm.nih.gov/pubmed/37707055
http://dx.doi.org/10.1128/msystems.00429-23
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author Peng, Kai
Li, Yangfan
Wang, Qiaojun
Yang, Pengbin
Wang, Zhiqiang
Li, Ruichao
author_facet Peng, Kai
Li, Yangfan
Wang, Qiaojun
Yang, Pengbin
Wang, Zhiqiang
Li, Ruichao
author_sort Peng, Kai
collection PubMed
description Integrative conjugative elements (ICEs) are important mobile elements that are associated with the dissemination of antibiotic resistance genes (ARGs) in Proteus. Recent studies demonstrated that the tigecycline resistance gene cluster tmexCD-toprJ has emerged in ICEs of Proteus. However, the prevalence of tmexCD-toprJ positive Proteus from animal sources is unclear. To cover the gap, a total of 762 Proteus spp. were isolated from animal source from six provinces of China to identify the tmexCD-toprJ positive isolates. Eight tmexCD-toprJ positive isolates were identified, with the tmexCD-toprJ positive rate of 1.05% against all Proteus spp. and 2.79% against ICE-bearing Proteus spp. The tmexCD-toprJ gene cluster in these Proteus spp. were tmexCD3-toprJ1b and all of them were carried by ICEs. Genetic structure analysis showed that tmexCD3-toprJ1b-bearing ICEs were complicated and plastic, but the tmexCD3-toprJ1b was specifically integrated into variable region III (VRIII) of ICEs with the help of integrases. Furthermore, we found that the umuC gene, which is presented in VRIII of ICEs and other genetic structures of many other bacterial genomes, was a hotspot for the integration of tmexCD-toprJ-bearing potential mobile elements. In summary, our results suggested that Proteus were important reservoirs for tmexCD-toprJ due to the high prevalence of ICEs. Therefore, continuous surveillance of ICEs-associated ARGs in Proteus is necessary and significant for controlling their future transmission. IMPORTANCE: The emergence and spread of tmexCD-toprJ have greatly weakened the function of tigecycline. Although studies have demonstrated the significance of Proteus as carriers for tmexCD-toprJ, the epidemic mechanism and characteristics of tmexCD-toprJ in Proteus remain unclear. Herein, we deciphered that the umuC gene in VRIII of SXT/R391 ICEs was a hotspot for the integration of tmexCD3-toprJ1b-bearing mobile genetic elements by genomic analysis. The mobilization and dissemination of tmexCD3-toprJ1b in Proteus were mediated by highly prevalent ICEs. Furthermore, the co-occurrence of tmexCD3-toprJ1b-bearing ICEs with other chromosomally encoded multidrug resistance gene islands warned that the chromosomes of Proteus are significant reservoirs of ARGs. Overall, our results provide significant insights for the prevention and control of tmexCD3-toprJ1b in Proteus.
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spelling pubmed-106540562023-09-14 Integrative conjugative elements mediate the high prevalence of tmexCD3-toprJ1b in Proteus spp. of animal source Peng, Kai Li, Yangfan Wang, Qiaojun Yang, Pengbin Wang, Zhiqiang Li, Ruichao mSystems Research Article Integrative conjugative elements (ICEs) are important mobile elements that are associated with the dissemination of antibiotic resistance genes (ARGs) in Proteus. Recent studies demonstrated that the tigecycline resistance gene cluster tmexCD-toprJ has emerged in ICEs of Proteus. However, the prevalence of tmexCD-toprJ positive Proteus from animal sources is unclear. To cover the gap, a total of 762 Proteus spp. were isolated from animal source from six provinces of China to identify the tmexCD-toprJ positive isolates. Eight tmexCD-toprJ positive isolates were identified, with the tmexCD-toprJ positive rate of 1.05% against all Proteus spp. and 2.79% against ICE-bearing Proteus spp. The tmexCD-toprJ gene cluster in these Proteus spp. were tmexCD3-toprJ1b and all of them were carried by ICEs. Genetic structure analysis showed that tmexCD3-toprJ1b-bearing ICEs were complicated and plastic, but the tmexCD3-toprJ1b was specifically integrated into variable region III (VRIII) of ICEs with the help of integrases. Furthermore, we found that the umuC gene, which is presented in VRIII of ICEs and other genetic structures of many other bacterial genomes, was a hotspot for the integration of tmexCD-toprJ-bearing potential mobile elements. In summary, our results suggested that Proteus were important reservoirs for tmexCD-toprJ due to the high prevalence of ICEs. Therefore, continuous surveillance of ICEs-associated ARGs in Proteus is necessary and significant for controlling their future transmission. IMPORTANCE: The emergence and spread of tmexCD-toprJ have greatly weakened the function of tigecycline. Although studies have demonstrated the significance of Proteus as carriers for tmexCD-toprJ, the epidemic mechanism and characteristics of tmexCD-toprJ in Proteus remain unclear. Herein, we deciphered that the umuC gene in VRIII of SXT/R391 ICEs was a hotspot for the integration of tmexCD3-toprJ1b-bearing mobile genetic elements by genomic analysis. The mobilization and dissemination of tmexCD3-toprJ1b in Proteus were mediated by highly prevalent ICEs. Furthermore, the co-occurrence of tmexCD3-toprJ1b-bearing ICEs with other chromosomally encoded multidrug resistance gene islands warned that the chromosomes of Proteus are significant reservoirs of ARGs. Overall, our results provide significant insights for the prevention and control of tmexCD3-toprJ1b in Proteus. American Society for Microbiology 2023-09-14 /pmc/articles/PMC10654056/ /pubmed/37707055 http://dx.doi.org/10.1128/msystems.00429-23 Text en Copyright © 2023 Peng 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
Peng, Kai
Li, Yangfan
Wang, Qiaojun
Yang, Pengbin
Wang, Zhiqiang
Li, Ruichao
Integrative conjugative elements mediate the high prevalence of tmexCD3-toprJ1b in Proteus spp. of animal source
title Integrative conjugative elements mediate the high prevalence of tmexCD3-toprJ1b in Proteus spp. of animal source
title_full Integrative conjugative elements mediate the high prevalence of tmexCD3-toprJ1b in Proteus spp. of animal source
title_fullStr Integrative conjugative elements mediate the high prevalence of tmexCD3-toprJ1b in Proteus spp. of animal source
title_full_unstemmed Integrative conjugative elements mediate the high prevalence of tmexCD3-toprJ1b in Proteus spp. of animal source
title_short Integrative conjugative elements mediate the high prevalence of tmexCD3-toprJ1b in Proteus spp. of animal source
title_sort integrative conjugative elements mediate the high prevalence of tmexcd3-toprj1b in proteus spp. of animal source
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10654056/
https://www.ncbi.nlm.nih.gov/pubmed/37707055
http://dx.doi.org/10.1128/msystems.00429-23
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