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Multidrug Resistance Plasmid pTZC1 Could Be Pooled among Cutibacterium Strains on the Skin Surface

Acne vulgaris is a chronic inflammatory skin disease that is exacerbated by Cutibacterium acnes. Although antimicrobials such as macrolides, clindamycin, and tetracyclines are used to treat acne caused by C. acnes, the increasing prevalence of antimicrobial-resistant C. acnes strains has become a gl...

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Autores principales: Koizumi, Juri, Nakase, Keisuke, Hayashi, Nobukazu, Takeo, Chikage, Nakaminami, Hidemasa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100872/
https://www.ncbi.nlm.nih.gov/pubmed/36847559
http://dx.doi.org/10.1128/spectrum.03628-22
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author Koizumi, Juri
Nakase, Keisuke
Hayashi, Nobukazu
Takeo, Chikage
Nakaminami, Hidemasa
author_facet Koizumi, Juri
Nakase, Keisuke
Hayashi, Nobukazu
Takeo, Chikage
Nakaminami, Hidemasa
author_sort Koizumi, Juri
collection PubMed
description Acne vulgaris is a chronic inflammatory skin disease that is exacerbated by Cutibacterium acnes. Although antimicrobials such as macrolides, clindamycin, and tetracyclines are used to treat acne caused by C. acnes, the increasing prevalence of antimicrobial-resistant C. acnes strains has become a global concern. In this study, we investigated the mechanism by which interspecies transfer of multidrug-resistant genes can lead to antimicrobial resistance. Specifically, the transfer of pTZC1 between C. acnes and C. granulosum isolated from specimens of patients with acne was investigated. Among the C. acnes and C. granulosum isolated from 10 patients with acne vulgaris, 60.0% and 70.0% of the isolates showed resistance to macrolides and clindamycin, respectively. The multidrug resistance plasmid pTZC1, which codes for macrolide-clindamycin resistance gene erm(50) and tetracycline resistance gene tet(W), was identified in both C. acnes and C. granulosum isolated from the same patient. In addition, whole-genome sequencing revealed that the pTZC1 sequences of C. acnes and C. granulosum showed 100% identity using comparative whole-genome sequencing analysis. Therefore, we hypothesize that the horizontal transfer of pTZC1 between C. acnes and C. granulosum strains may occur on the skin surface. The plasmid transfer test revealed a bidirectional transfer of pTZC1 between C. acnes and C. granulosum, and transconjugants that obtained pTZC1 exhibited multidrug resistance. In conclusion, our results revealed that the multidrug resistance plasmid pTZC1 could be transferred between C. acnes and C. granulosum. Furthermore, since pTZC1 transfer among different species may aid in the prevalence of multidrug resistant strains, antimicrobial resistance genes may have been pooled on the skin surface. IMPORTANCE The emergence of antimicrobial resistance not only in Cutibacterium acnes strain but also other skin bacteria such as Staphylococcus epidermidis is a big concern due to antimicrobial use for the treatment of acne vulgaris. Increased prevalence of macrolides-clindamycin resistant C. acnes relates to the acquisition of exogenous antimicrobial resistance genes. erm(50) is harbored by the multidrug resistance plasmid pTZC1, which has been found in C. acnes and C. granulosum strains isolated from patients with acne vulgaris. In this study, C. acnes and C. granulosum with pTZC1 were found in the same patient, and plasmid transfer between C. acnes and C. granulosum was proved by transconjugation assay. This study showed plasmid transfer between other species and the possibility of further prevalence antimicrobial resistance between Cutibacterium species.
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spelling pubmed-101008722023-04-14 Multidrug Resistance Plasmid pTZC1 Could Be Pooled among Cutibacterium Strains on the Skin Surface Koizumi, Juri Nakase, Keisuke Hayashi, Nobukazu Takeo, Chikage Nakaminami, Hidemasa Microbiol Spectr Research Article Acne vulgaris is a chronic inflammatory skin disease that is exacerbated by Cutibacterium acnes. Although antimicrobials such as macrolides, clindamycin, and tetracyclines are used to treat acne caused by C. acnes, the increasing prevalence of antimicrobial-resistant C. acnes strains has become a global concern. In this study, we investigated the mechanism by which interspecies transfer of multidrug-resistant genes can lead to antimicrobial resistance. Specifically, the transfer of pTZC1 between C. acnes and C. granulosum isolated from specimens of patients with acne was investigated. Among the C. acnes and C. granulosum isolated from 10 patients with acne vulgaris, 60.0% and 70.0% of the isolates showed resistance to macrolides and clindamycin, respectively. The multidrug resistance plasmid pTZC1, which codes for macrolide-clindamycin resistance gene erm(50) and tetracycline resistance gene tet(W), was identified in both C. acnes and C. granulosum isolated from the same patient. In addition, whole-genome sequencing revealed that the pTZC1 sequences of C. acnes and C. granulosum showed 100% identity using comparative whole-genome sequencing analysis. Therefore, we hypothesize that the horizontal transfer of pTZC1 between C. acnes and C. granulosum strains may occur on the skin surface. The plasmid transfer test revealed a bidirectional transfer of pTZC1 between C. acnes and C. granulosum, and transconjugants that obtained pTZC1 exhibited multidrug resistance. In conclusion, our results revealed that the multidrug resistance plasmid pTZC1 could be transferred between C. acnes and C. granulosum. Furthermore, since pTZC1 transfer among different species may aid in the prevalence of multidrug resistant strains, antimicrobial resistance genes may have been pooled on the skin surface. IMPORTANCE The emergence of antimicrobial resistance not only in Cutibacterium acnes strain but also other skin bacteria such as Staphylococcus epidermidis is a big concern due to antimicrobial use for the treatment of acne vulgaris. Increased prevalence of macrolides-clindamycin resistant C. acnes relates to the acquisition of exogenous antimicrobial resistance genes. erm(50) is harbored by the multidrug resistance plasmid pTZC1, which has been found in C. acnes and C. granulosum strains isolated from patients with acne vulgaris. In this study, C. acnes and C. granulosum with pTZC1 were found in the same patient, and plasmid transfer between C. acnes and C. granulosum was proved by transconjugation assay. This study showed plasmid transfer between other species and the possibility of further prevalence antimicrobial resistance between Cutibacterium species. American Society for Microbiology 2023-02-27 /pmc/articles/PMC10100872/ /pubmed/36847559 http://dx.doi.org/10.1128/spectrum.03628-22 Text en Copyright © 2023 Koizumi 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
Koizumi, Juri
Nakase, Keisuke
Hayashi, Nobukazu
Takeo, Chikage
Nakaminami, Hidemasa
Multidrug Resistance Plasmid pTZC1 Could Be Pooled among Cutibacterium Strains on the Skin Surface
title Multidrug Resistance Plasmid pTZC1 Could Be Pooled among Cutibacterium Strains on the Skin Surface
title_full Multidrug Resistance Plasmid pTZC1 Could Be Pooled among Cutibacterium Strains on the Skin Surface
title_fullStr Multidrug Resistance Plasmid pTZC1 Could Be Pooled among Cutibacterium Strains on the Skin Surface
title_full_unstemmed Multidrug Resistance Plasmid pTZC1 Could Be Pooled among Cutibacterium Strains on the Skin Surface
title_short Multidrug Resistance Plasmid pTZC1 Could Be Pooled among Cutibacterium Strains on the Skin Surface
title_sort multidrug resistance plasmid ptzc1 could be pooled among cutibacterium strains on the skin surface
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100872/
https://www.ncbi.nlm.nih.gov/pubmed/36847559
http://dx.doi.org/10.1128/spectrum.03628-22
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