WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome

Mette Pinholt; Sion C Bayliss; Heidi Gumpert; Peder Worning; Veronika V S Jensen; Michael Pedersen; Edward J Feil; Henrik Westh

doi:10.1093/jac/dkz118

WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome

Mette Pinholt, Sion C Bayliss, Heidi Gumpert, Peder Worning, Veronika V S Jensen, Michael Pedersen, Edward J Feil, Henrik Westh

Department of Clinical Medicine

13 Citations (Scopus)

Abstract

OBJECTIVES: From 2012 to 2015, a sudden significant increase in vancomycin-resistant (vanA) Enterococcus faecium (VREfm) was observed in the Capital Region of Denmark. Clonal relatedness of VREfm and vancomycin-susceptible E. faecium (VSEfm) was investigated, transmission events between hospitals were identified and the pan-genome and plasmids from the largest VREfm clonal group were characterized.

METHODS: WGS of 1058 E. faecium isolates was carried out on the Illumina platform to perform SNP analysis and to identify the pan-genome. One isolate was also sequenced on the PacBio platform to close the genome. Epidemiological data were collected from laboratory information systems.

RESULTS: Phylogeny of 892 VREfm and 166 VSEfm revealed a polyclonal structure, with a single clonal group (ST80) accounting for 40% of the VREfm isolates. VREfm and VSEfm co-occurred within many clonal groups; however, no VSEfm were related to the dominant VREfm group. A similar vanA plasmid was identified in ≥99% of isolates belonging to the dominant group and 69% of the remaining VREfm. Ten plasmids were identified in the completed genome, and ∼29% of this genome consisted of dispensable accessory genes. The size of the pan-genome among isolates in the dominant group was 5905 genes.

CONCLUSIONS: Most probably, VREfm emerged owing to importation of a successful VREfm clone which rapidly transmitted to the majority of hospitals in the region whilst simultaneously disseminating a vanA plasmid to pre-existing VSEfm. Acquisition of a heterogeneous accessory genome may account for the success of this clone by facilitating adaptation to new environmental challenges.

Original language	English
Journal	The Journal of antimicrobial chemotherapy
Volume	74
Issue number	7
Pages (from-to)	1776-1785
ISSN	0305-7453
DOIs	https://doi.org/10.1093/jac/dkz118
Publication status	Published - 1 Jul 2019

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Pinholt, M., Bayliss, S. C., Gumpert, H., Worning, P., Jensen, V. V. S., Pedersen, M., Feil, E. J., & Westh, H. (2019). WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome. The Journal of antimicrobial chemotherapy, 74(7), 1776-1785. https://doi.org/10.1093/jac/dkz118

WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome. / Pinholt, Mette; Bayliss, Sion C; Gumpert, Heidi et al.
In: The Journal of antimicrobial chemotherapy, Vol. 74, No. 7, 01.07.2019, p. 1776-1785.

Research output: Contribution to journal › Journal article › Research › peer-review

Pinholt, M, Bayliss, SC, Gumpert, H, Worning, P, Jensen, VVS, Pedersen, M, Feil, EJ & Westh, H 2019, 'WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome', The Journal of antimicrobial chemotherapy, vol. 74, no. 7, pp. 1776-1785. https://doi.org/10.1093/jac/dkz118

Pinholt M, Bayliss SC, Gumpert H, Worning P, Jensen VVS, Pedersen M et al. WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome. The Journal of antimicrobial chemotherapy. 2019 Jul 1;74(7):1776-1785. doi: 10.1093/jac/dkz118

Pinholt, Mette ; Bayliss, Sion C ; Gumpert, Heidi et al. / WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome. In: The Journal of antimicrobial chemotherapy. 2019 ; Vol. 74, No. 7. pp. 1776-1785.

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title = "WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome",

abstract = "OBJECTIVES: From 2012 to 2015, a sudden significant increase in vancomycin-resistant (vanA) Enterococcus faecium (VREfm) was observed in the Capital Region of Denmark. Clonal relatedness of VREfm and vancomycin-susceptible E. faecium (VSEfm) was investigated, transmission events between hospitals were identified and the pan-genome and plasmids from the largest VREfm clonal group were characterized.METHODS: WGS of 1058 E. faecium isolates was carried out on the Illumina platform to perform SNP analysis and to identify the pan-genome. One isolate was also sequenced on the PacBio platform to close the genome. Epidemiological data were collected from laboratory information systems.RESULTS: Phylogeny of 892 VREfm and 166 VSEfm revealed a polyclonal structure, with a single clonal group (ST80) accounting for 40% of the VREfm isolates. VREfm and VSEfm co-occurred within many clonal groups; however, no VSEfm were related to the dominant VREfm group. A similar vanA plasmid was identified in ≥99% of isolates belonging to the dominant group and 69% of the remaining VREfm. Ten plasmids were identified in the completed genome, and ∼29% of this genome consisted of dispensable accessory genes. The size of the pan-genome among isolates in the dominant group was 5905 genes.CONCLUSIONS: Most probably, VREfm emerged owing to importation of a successful VREfm clone which rapidly transmitted to the majority of hospitals in the region whilst simultaneously disseminating a vanA plasmid to pre-existing VSEfm. Acquisition of a heterogeneous accessory genome may account for the success of this clone by facilitating adaptation to new environmental challenges.",

author = "Mette Pinholt and Bayliss, {Sion C} and Heidi Gumpert and Peder Worning and Jensen, {Veronika V S} and Michael Pedersen and Feil, {Edward J} and Henrik Westh",

note = "{\textcopyright} The Author(s) 2019. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For permissions, please email: [email protected].",

year = "2019",

month = jul,

day = "1",

doi = "10.1093/jac/dkz118",

language = "English",

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T1 - WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome

AU - Pinholt, Mette

AU - Bayliss, Sion C

AU - Gumpert, Heidi

AU - Worning, Peder

AU - Jensen, Veronika V S

AU - Pedersen, Michael

AU - Feil, Edward J

AU - Westh, Henrik

PY - 2019/7/1

Y1 - 2019/7/1

N2 - OBJECTIVES: From 2012 to 2015, a sudden significant increase in vancomycin-resistant (vanA) Enterococcus faecium (VREfm) was observed in the Capital Region of Denmark. Clonal relatedness of VREfm and vancomycin-susceptible E. faecium (VSEfm) was investigated, transmission events between hospitals were identified and the pan-genome and plasmids from the largest VREfm clonal group were characterized.METHODS: WGS of 1058 E. faecium isolates was carried out on the Illumina platform to perform SNP analysis and to identify the pan-genome. One isolate was also sequenced on the PacBio platform to close the genome. Epidemiological data were collected from laboratory information systems.RESULTS: Phylogeny of 892 VREfm and 166 VSEfm revealed a polyclonal structure, with a single clonal group (ST80) accounting for 40% of the VREfm isolates. VREfm and VSEfm co-occurred within many clonal groups; however, no VSEfm were related to the dominant VREfm group. A similar vanA plasmid was identified in ≥99% of isolates belonging to the dominant group and 69% of the remaining VREfm. Ten plasmids were identified in the completed genome, and ∼29% of this genome consisted of dispensable accessory genes. The size of the pan-genome among isolates in the dominant group was 5905 genes.CONCLUSIONS: Most probably, VREfm emerged owing to importation of a successful VREfm clone which rapidly transmitted to the majority of hospitals in the region whilst simultaneously disseminating a vanA plasmid to pre-existing VSEfm. Acquisition of a heterogeneous accessory genome may account for the success of this clone by facilitating adaptation to new environmental challenges.

AB - OBJECTIVES: From 2012 to 2015, a sudden significant increase in vancomycin-resistant (vanA) Enterococcus faecium (VREfm) was observed in the Capital Region of Denmark. Clonal relatedness of VREfm and vancomycin-susceptible E. faecium (VSEfm) was investigated, transmission events between hospitals were identified and the pan-genome and plasmids from the largest VREfm clonal group were characterized.METHODS: WGS of 1058 E. faecium isolates was carried out on the Illumina platform to perform SNP analysis and to identify the pan-genome. One isolate was also sequenced on the PacBio platform to close the genome. Epidemiological data were collected from laboratory information systems.RESULTS: Phylogeny of 892 VREfm and 166 VSEfm revealed a polyclonal structure, with a single clonal group (ST80) accounting for 40% of the VREfm isolates. VREfm and VSEfm co-occurred within many clonal groups; however, no VSEfm were related to the dominant VREfm group. A similar vanA plasmid was identified in ≥99% of isolates belonging to the dominant group and 69% of the remaining VREfm. Ten plasmids were identified in the completed genome, and ∼29% of this genome consisted of dispensable accessory genes. The size of the pan-genome among isolates in the dominant group was 5905 genes.CONCLUSIONS: Most probably, VREfm emerged owing to importation of a successful VREfm clone which rapidly transmitted to the majority of hospitals in the region whilst simultaneously disseminating a vanA plasmid to pre-existing VSEfm. Acquisition of a heterogeneous accessory genome may account for the success of this clone by facilitating adaptation to new environmental challenges.

U2 - 10.1093/jac/dkz118

DO - 10.1093/jac/dkz118

M3 - Journal article

C2 - 30929020

SN - 0305-7453

VL - 74

SP - 1776

EP - 1785

JO - The Journal of antimicrobial chemotherapy

JF - The Journal of antimicrobial chemotherapy

IS - 7

ER -