Genomic Stability of Composite SCCmec ACME and COMER-Like Genetic Elements in Staphylococcus epidermidis Correlates With Rate of Excision

Nada Almebairik; Roxana Zamudio; Chaitanya Joshi; Corinne Ironside; Joseph D. Ralph; Adam P. Roberts; Ian M. Gould; Julie A. Morrissey; Karolin Hijazi; Marco R. Oggioni

doi:10.3389/fmicb.2020.00166

Genomic Stability of Composite SCCmec ACME and COMER-Like Genetic Elements in Staphylococcus epidermidis Correlates With Rate of Excision

Nada Almebairik, Roxana Zamudio, Chaitanya Joshi, Corinne Ironside, Joseph D. Ralph, Adam P. Roberts, Ian M. Gould, Julie A. Morrissey, Karolin Hijazi, Marco R. Oggioni^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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Abstract

The epidemiological success of methicillin-resistant Staphylococcus aureus USA300 has been associated with the presence of two mobile elements, the arginine catabolic mobile element (ACME) and the copper and mercury resistance (COMER) element. These two mobile elements are associated with resistance to copper, which has been related to host fitness and survival within macrophages. Several studies found that ACME is more prevalent, and exhibits greater diversity, in Staphylococcus epidermidis while COMER has not been identified in S. epidermidis or any other staphylococcal species. We aimed in this study to evaluate the presence and diversity of ACME and COMER-like elements in our S. epidermidis clinical isolates. The genomes of 58 S. epidermidis clinical isolates, collected between 2009 and 2018 in a Scottish hospital, were sequenced. A core-genome phylogenetic tree and genome based MLST typing showed that more than half of the isolates belong to the clinically predominant sequence type2 (ST2) and these isolates have been found to split into two lineages within the phylogenetic tree. Analysis showed the presence of SCCmec in the majority of isolates. Comparative analysis identified a cluster of ACME-positive isolates with most of them belonging to ST48. ACME showed high variation even between isolates of the same ACME type and ST. COMER-like elements have been identified in one of the two major hospital adapted drug resistant ST2 lineages; and showed high stability. This difference in stability at the genomic level correlates well with the up to one hundred times higher excision frequency found for the SCCmec elements in ACME-containing isolates compared to COMER-like element containing isolates. ACME / COMER-like element positive isolates did not show a significant phenotype of decreased copper susceptibility, while resistance to mercury was over-represented in COMER-like element positive isolates. To the best of our knowledge, this is the first molecular characterization of COMER-like elements in S. epidermidis isolates. The presence of the COMER-like elements is the most prominent accessory genome feature of these successful lineages suggesting that this chromosomal island contributes to the success and wide clinical distribution of ST2 S. epidermidis.

Original language	English
Article number	166
Number of pages	12
Journal	Frontiers in Microbiology
Volume	11
DOIs	https://doi.org/10.3389/fmicb.2020.00166
Publication status	Published - 12 Feb 2020

Bibliographical note

NA is supported by a fellowship of the King Saud University (Riyadh, Saudi Arabia). The authors thank the work of the management team of the ALICE High Performance Computing Facility at the University of Leicester. JDR is supported by the BBSRC grant BB/P504737/1.

Data AvailabiliTy Statement
The datasets generated for this study can be found in the GenBank (accession numbers SAMN12840193–SAMN12840250).

Keywords

Staphylococcus epidermidis
Mobile genetic element
ACME
COMER
SCCmec
mobile genetic element
CATABOLIC MOBILE ELEMENT
PREVALENCE
ALIGNMENT
DNA
SEQUENCE
RESISTANCE
TOOL

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Almebairik_etal_fmicb_genomic_stability_VOR
© 2020 Almebairik, Zamudio, Ironside, Joshi, Ralph, Roberts, Gould, Morrissey, Hijazi and Oggioni. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. https://creativecommons.org/licenses/by/4.0/
Final published version, 9.22 MBLicence: CC BY

Cite this

Almebairik, N., Zamudio, R., Joshi, C., Ironside, C., Ralph, J. D., Roberts, A. P., Gould, I. M., Morrissey, J. A., Hijazi, K., & Oggioni, M. R. (2020). Genomic Stability of Composite SCCmec ACME and COMER-Like Genetic Elements in Staphylococcus epidermidis Correlates With Rate of Excision. Frontiers in Microbiology, 11, Article 166. https://doi.org/10.3389/fmicb.2020.00166

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title = "Genomic Stability of Composite SCCmec ACME and COMER-Like Genetic Elements in Staphylococcus epidermidis Correlates With Rate of Excision",

abstract = "The epidemiological success of methicillin-resistant Staphylococcus aureus USA300 has been associated with the presence of two mobile elements, the arginine catabolic mobile element (ACME) and the copper and mercury resistance (COMER) element. These two mobile elements are associated with resistance to copper, which has been related to host fitness and survival within macrophages. Several studies found that ACME is more prevalent, and exhibits greater diversity, in Staphylococcus epidermidis while COMER has not been identified in S. epidermidis or any other staphylococcal species. We aimed in this study to evaluate the presence and diversity of ACME and COMER-like elements in our S. epidermidis clinical isolates. The genomes of 58 S. epidermidis clinical isolates, collected between 2009 and 2018 in a Scottish hospital, were sequenced. A core-genome phylogenetic tree and genome based MLST typing showed that more than half of the isolates belong to the clinically predominant sequence type2 (ST2) and these isolates have been found to split into two lineages within the phylogenetic tree. Analysis showed the presence of SCCmec in the majority of isolates. Comparative analysis identified a cluster of ACME-positive isolates with most of them belonging to ST48. ACME showed high variation even between isolates of the same ACME type and ST. COMER-like elements have been identified in one of the two major hospital adapted drug resistant ST2 lineages; and showed high stability. This difference in stability at the genomic level correlates well with the up to one hundred times higher excision frequency found for the SCCmec elements in ACME-containing isolates compared to COMER-like element containing isolates. ACME / COMER-like element positive isolates did not show a significant phenotype of decreased copper susceptibility, while resistance to mercury was over-represented in COMER-like element positive isolates. To the best of our knowledge, this is the first molecular characterization of COMER-like elements in S. epidermidis isolates. The presence of the COMER-like elements is the most prominent accessory genome feature of these successful lineages suggesting that this chromosomal island contributes to the success and wide clinical distribution of ST2 S. epidermidis.",

keywords = "Staphylococcus epidermidis, Mobile genetic element, ACME, COMER, SCCmec, mobile genetic element, CATABOLIC MOBILE ELEMENT, PREVALENCE, ALIGNMENT, DNA, SEQUENCE, RESISTANCE, TOOL",

author = "Nada Almebairik and Roxana Zamudio and Chaitanya Joshi and Corinne Ironside and Ralph, {Joseph D.} and Roberts, {Adam P.} and Gould, {Ian M.} and Morrissey, {Julie A.} and Karolin Hijazi and Oggioni, {Marco R.}",

note = "NA is supported by a fellowship of the King Saud University (Riyadh, Saudi Arabia). The authors thank the work of the management team of the ALICE High Performance Computing Facility at the University of Leicester. JDR is supported by the BBSRC grant BB/P504737/1. Data AvailabiliTy Statement The datasets generated for this study can be found in the GenBank (accession numbers SAMN12840193–SAMN12840250).",

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AU - Almebairik, Nada

AU - Zamudio, Roxana

AU - Joshi, Chaitanya

AU - Ironside, Corinne

AU - Ralph, Joseph D.

AU - Roberts, Adam P.

AU - Gould, Ian M.

AU - Morrissey, Julie A.

AU - Hijazi, Karolin

AU - Oggioni, Marco R.

N1 - NA is supported by a fellowship of the King Saud University (Riyadh, Saudi Arabia). The authors thank the work of the management team of the ALICE High Performance Computing Facility at the University of Leicester. JDR is supported by the BBSRC grant BB/P504737/1. Data AvailabiliTy Statement The datasets generated for this study can be found in the GenBank (accession numbers SAMN12840193–SAMN12840250).

PY - 2020/2/12

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N2 - The epidemiological success of methicillin-resistant Staphylococcus aureus USA300 has been associated with the presence of two mobile elements, the arginine catabolic mobile element (ACME) and the copper and mercury resistance (COMER) element. These two mobile elements are associated with resistance to copper, which has been related to host fitness and survival within macrophages. Several studies found that ACME is more prevalent, and exhibits greater diversity, in Staphylococcus epidermidis while COMER has not been identified in S. epidermidis or any other staphylococcal species. We aimed in this study to evaluate the presence and diversity of ACME and COMER-like elements in our S. epidermidis clinical isolates. The genomes of 58 S. epidermidis clinical isolates, collected between 2009 and 2018 in a Scottish hospital, were sequenced. A core-genome phylogenetic tree and genome based MLST typing showed that more than half of the isolates belong to the clinically predominant sequence type2 (ST2) and these isolates have been found to split into two lineages within the phylogenetic tree. Analysis showed the presence of SCCmec in the majority of isolates. Comparative analysis identified a cluster of ACME-positive isolates with most of them belonging to ST48. ACME showed high variation even between isolates of the same ACME type and ST. COMER-like elements have been identified in one of the two major hospital adapted drug resistant ST2 lineages; and showed high stability. This difference in stability at the genomic level correlates well with the up to one hundred times higher excision frequency found for the SCCmec elements in ACME-containing isolates compared to COMER-like element containing isolates. ACME / COMER-like element positive isolates did not show a significant phenotype of decreased copper susceptibility, while resistance to mercury was over-represented in COMER-like element positive isolates. To the best of our knowledge, this is the first molecular characterization of COMER-like elements in S. epidermidis isolates. The presence of the COMER-like elements is the most prominent accessory genome feature of these successful lineages suggesting that this chromosomal island contributes to the success and wide clinical distribution of ST2 S. epidermidis.

AB - The epidemiological success of methicillin-resistant Staphylococcus aureus USA300 has been associated with the presence of two mobile elements, the arginine catabolic mobile element (ACME) and the copper and mercury resistance (COMER) element. These two mobile elements are associated with resistance to copper, which has been related to host fitness and survival within macrophages. Several studies found that ACME is more prevalent, and exhibits greater diversity, in Staphylococcus epidermidis while COMER has not been identified in S. epidermidis or any other staphylococcal species. We aimed in this study to evaluate the presence and diversity of ACME and COMER-like elements in our S. epidermidis clinical isolates. The genomes of 58 S. epidermidis clinical isolates, collected between 2009 and 2018 in a Scottish hospital, were sequenced. A core-genome phylogenetic tree and genome based MLST typing showed that more than half of the isolates belong to the clinically predominant sequence type2 (ST2) and these isolates have been found to split into two lineages within the phylogenetic tree. Analysis showed the presence of SCCmec in the majority of isolates. Comparative analysis identified a cluster of ACME-positive isolates with most of them belonging to ST48. ACME showed high variation even between isolates of the same ACME type and ST. COMER-like elements have been identified in one of the two major hospital adapted drug resistant ST2 lineages; and showed high stability. This difference in stability at the genomic level correlates well with the up to one hundred times higher excision frequency found for the SCCmec elements in ACME-containing isolates compared to COMER-like element containing isolates. ACME / COMER-like element positive isolates did not show a significant phenotype of decreased copper susceptibility, while resistance to mercury was over-represented in COMER-like element positive isolates. To the best of our knowledge, this is the first molecular characterization of COMER-like elements in S. epidermidis isolates. The presence of the COMER-like elements is the most prominent accessory genome feature of these successful lineages suggesting that this chromosomal island contributes to the success and wide clinical distribution of ST2 S. epidermidis.

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KW - COMER

KW - SCCmec

KW - mobile genetic element

KW - CATABOLIC MOBILE ELEMENT

KW - PREVALENCE

KW - ALIGNMENT

KW - DNA

KW - SEQUENCE

KW - RESISTANCE

KW - TOOL

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U2 - 10.3389/fmicb.2020.00166

DO - 10.3389/fmicb.2020.00166

M3 - Article

SN - 1664-302X

VL - 11

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

M1 - 166

ER -

Genomic Stability of Composite SCCmec ACME and COMER-Like Genetic Elements in Staphylococcus epidermidis Correlates With Rate of Excision

Abstract

Bibliographical note

Keywords

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Karolin Hijazi

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Genomic Stability of Composite SCCmec ACME and COMER-Like Genetic Elements in Staphylococcus epidermidis Correlates With Rate of Excision

Abstract

Bibliographical note

Keywords

Access to Document

Other files and links

Fingerprint

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Karolin Hijazi

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