First Report of the Local Spread of Vancomycin-Resistant Enterococci Ascribed to the Interspecies Transmission of a <italic toggle="yes">vanA</italic> Gene Cluster-Carrying Linear Plasmid

ABSTRACT Vancomycin-resistant enterococci pose a threat in the clinical setting and have been linked to hospital outbreaks worldwide. In 2017, a local spread of VanA-type vancomycin-resistant enterococci (VRE) occurred in Japan, and 25 enterococcal isolates, including 14 Enterococcus faecium, 8 E. r...

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Autores principales: Yusuke Hashimoto, Izumi Kita, Masato Suzuki, Hidetada Hirakawa, Hirofumi Ohtaki, Haruyoshi Tomita
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:1692b5982475427995214626ca58adc52021-11-15T15:29:16ZFirst Report of the Local Spread of Vancomycin-Resistant Enterococci Ascribed to the Interspecies Transmission of a <italic toggle="yes">vanA</italic> Gene Cluster-Carrying Linear Plasmid10.1128/mSphere.00102-202379-5042https://doaj.org/article/1692b5982475427995214626ca58adc52020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00102-20https://doaj.org/toc/2379-5042ABSTRACT Vancomycin-resistant enterococci pose a threat in the clinical setting and have been linked to hospital outbreaks worldwide. In 2017, a local spread of VanA-type vancomycin-resistant enterococci (VRE) occurred in Japan, and 25 enterococcal isolates, including 14 Enterococcus faecium, 8 E. raffinosus, and 3 E. casseliflavus isolates, were identified from four inpatients. Molecular analysis of the multispecies of VanA-type VRE revealed the involvement of both the dissemination of clonally related VRE strains between patients and the horizontal transfer of plasmids harboring the vanA gene cluster between Enterococcus spp. Pulsed-field gel electrophoresis showed that the plasmid DNAs without S1 nuclease treatment were able to migrate into the gel, suggesting that the topology of the plasmid was linear. Whole-genome sequencing revealed that this plasmid, designated pELF2, was 108,102 bp long and encoded multiple antimicrobial resistance genes, including ermA and ant(9). The amino acid sequences of putative replication- and transfer-related genes were highly conserved between pELF2 and pELF1, the latter of which was the first identified enterococcal conjugative linear plasmid. On comparing the genomic structure, pELF2 showed the presence of a backbone similar to that of pELF1, especially with respect to the nucleotide sequences of both terminal ends, indicating a hybrid-type linear plasmid, possessing two different terminal structures. pELF2 possessed a broad host range and high conjugation frequencies for enterococci. The easy transfer of pELF2 to different Enterococcus spp. in vitro might explain this local spread of multiple species, highlighting the clinical threat from the spread of antimicrobial resistance by an enterococcal linear plasmid. IMPORTANCE Increasing multidrug resistance, including vancomycin resistance, in enterococci is a major concern in clinical settings. Horizontal gene transfer, such as via plasmids, has been shown to play a crucial role in the acquisition of vancomycin resistance. Among vancomycin resistance types, the VanA type is one of the most prevalent, and outbreaks caused by VanA-type vancomycin-resistant enterococci (VRE) have occurred worldwide. Here, we describe an enterococcal linear plasmid responsible for multispecies local spread of VanA-type VRE. Such a study is important because although hospital outbreaks caused by mixed enterococcal species have been reported, this particular spread indicates plasmid transfer across species. This is a crucial finding because the high risk for such a spread of antimicrobial resistance calls for regular monitoring and surveillance.Yusuke HashimotoIzumi KitaMasato SuzukiHidetada HirakawaHirofumi OhtakiHaruyoshi TomitaAmerican Society for Microbiologyarticlevancomycin-resistant enterococciconjugative linear plasmidlocal spreadinterspecies transmissionMicrobiologyQR1-502ENmSphere, Vol 5, Iss 2 (2020)
institution DOAJ
collection DOAJ
language EN
topic vancomycin-resistant enterococci
conjugative linear plasmid
local spread
interspecies transmission
Microbiology
QR1-502
spellingShingle vancomycin-resistant enterococci
conjugative linear plasmid
local spread
interspecies transmission
Microbiology
QR1-502
Yusuke Hashimoto
Izumi Kita
Masato Suzuki
Hidetada Hirakawa
Hirofumi Ohtaki
Haruyoshi Tomita
First Report of the Local Spread of Vancomycin-Resistant Enterococci Ascribed to the Interspecies Transmission of a <italic toggle="yes">vanA</italic> Gene Cluster-Carrying Linear Plasmid
description ABSTRACT Vancomycin-resistant enterococci pose a threat in the clinical setting and have been linked to hospital outbreaks worldwide. In 2017, a local spread of VanA-type vancomycin-resistant enterococci (VRE) occurred in Japan, and 25 enterococcal isolates, including 14 Enterococcus faecium, 8 E. raffinosus, and 3 E. casseliflavus isolates, were identified from four inpatients. Molecular analysis of the multispecies of VanA-type VRE revealed the involvement of both the dissemination of clonally related VRE strains between patients and the horizontal transfer of plasmids harboring the vanA gene cluster between Enterococcus spp. Pulsed-field gel electrophoresis showed that the plasmid DNAs without S1 nuclease treatment were able to migrate into the gel, suggesting that the topology of the plasmid was linear. Whole-genome sequencing revealed that this plasmid, designated pELF2, was 108,102 bp long and encoded multiple antimicrobial resistance genes, including ermA and ant(9). The amino acid sequences of putative replication- and transfer-related genes were highly conserved between pELF2 and pELF1, the latter of which was the first identified enterococcal conjugative linear plasmid. On comparing the genomic structure, pELF2 showed the presence of a backbone similar to that of pELF1, especially with respect to the nucleotide sequences of both terminal ends, indicating a hybrid-type linear plasmid, possessing two different terminal structures. pELF2 possessed a broad host range and high conjugation frequencies for enterococci. The easy transfer of pELF2 to different Enterococcus spp. in vitro might explain this local spread of multiple species, highlighting the clinical threat from the spread of antimicrobial resistance by an enterococcal linear plasmid. IMPORTANCE Increasing multidrug resistance, including vancomycin resistance, in enterococci is a major concern in clinical settings. Horizontal gene transfer, such as via plasmids, has been shown to play a crucial role in the acquisition of vancomycin resistance. Among vancomycin resistance types, the VanA type is one of the most prevalent, and outbreaks caused by VanA-type vancomycin-resistant enterococci (VRE) have occurred worldwide. Here, we describe an enterococcal linear plasmid responsible for multispecies local spread of VanA-type VRE. Such a study is important because although hospital outbreaks caused by mixed enterococcal species have been reported, this particular spread indicates plasmid transfer across species. This is a crucial finding because the high risk for such a spread of antimicrobial resistance calls for regular monitoring and surveillance.
format article
author Yusuke Hashimoto
Izumi Kita
Masato Suzuki
Hidetada Hirakawa
Hirofumi Ohtaki
Haruyoshi Tomita
author_facet Yusuke Hashimoto
Izumi Kita
Masato Suzuki
Hidetada Hirakawa
Hirofumi Ohtaki
Haruyoshi Tomita
author_sort Yusuke Hashimoto
title First Report of the Local Spread of Vancomycin-Resistant Enterococci Ascribed to the Interspecies Transmission of a <italic toggle="yes">vanA</italic> Gene Cluster-Carrying Linear Plasmid
title_short First Report of the Local Spread of Vancomycin-Resistant Enterococci Ascribed to the Interspecies Transmission of a <italic toggle="yes">vanA</italic> Gene Cluster-Carrying Linear Plasmid
title_full First Report of the Local Spread of Vancomycin-Resistant Enterococci Ascribed to the Interspecies Transmission of a <italic toggle="yes">vanA</italic> Gene Cluster-Carrying Linear Plasmid
title_fullStr First Report of the Local Spread of Vancomycin-Resistant Enterococci Ascribed to the Interspecies Transmission of a <italic toggle="yes">vanA</italic> Gene Cluster-Carrying Linear Plasmid
title_full_unstemmed First Report of the Local Spread of Vancomycin-Resistant Enterococci Ascribed to the Interspecies Transmission of a <italic toggle="yes">vanA</italic> Gene Cluster-Carrying Linear Plasmid
title_sort first report of the local spread of vancomycin-resistant enterococci ascribed to the interspecies transmission of a <italic toggle="yes">vana</italic> gene cluster-carrying linear plasmid
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/1692b5982475427995214626ca58adc5
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