Detection and characterisation of 16S rRNA methyltransferase-producing Pseudomonas aeruginosa from the UK and Republic of Ireland from 2003–2015

Emma Taylor; Elita Jauneikaite; Shiranee Sriskandan; Neil Woodford; Katie L. Hopkins

doi:10.1016/j.ijantimicag.2022.106550

Detection and characterisation of 16S rRNA methyltransferase-producing Pseudomonas aeruginosa from the UK and Republic of Ireland from 2003–2015

Emma Taylor, Elita Jauneikaite, Shiranee Sriskandan, Neil Woodford, Katie L. Hopkins^*

^*Corresponding author for this work

UK Health Security Agency

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

7 Citations (Scopus)

Abstract

16S rRNA methyltransferase (16S RMTase) genes confer high-level aminoglycoside resistance, reducing treatment options for multidrug-resistant Gram-negative bacteria. Pseudomonas aeruginosa isolates (n = 221) exhibiting high-level pan-aminoglycoside resistance (amikacin, gentamicin and tobramycin MICs ≥64, ≥32 and ≥32 mg/L, respectively) were screened for 16S RMTase genes to determine their occurrence among isolates submitted to a national reference laboratory from December 2003 to December 2015. 16S RMTase genes were identified using two multiplex PCRs, and whole-genome sequencing (WGS) was used to identify other antibiotic resistance genes, sequence types (STs) and the genetic environment of 16S RMTase genes. 16S RMTase genes were found in 8.6% (19/221) of isolates, with rmtB4 (47.4%; 9/19) being most common, followed by rmtD3 (21.1%; 4/19), rmtF2 (15.8%; 3/19) and single isolates harbouring rmtB1, rmtC and rmtD1. Carbapenemase genes were found in 89.5% (17/19) of 16S RMTase-positive isolates, with bla_VIM (52.9%; 9/17) being most common. 16S RMTase genes were found in ‘high-risk’ clones known to harbour carbapenemase genes (ST233, ST277, ST357, ST654 and ST773). Analysis of the genetic environment of 16S RMTase genes identified that IS6100 was genetically linked to rmtB1; IS91 to rmtB4, rmtC or rmtD3; ISCR14 to rmtD1; and rmtF2 was linked to Tn3, IS91 or Tn1721. Although 16S RMTase genes explained only 8.6% of pan-aminoglycoside resistance in the P. aeruginosa isolates studied, the association of 16S RMTase genes with carbapenemase-producers and ‘high-risk’ clones highlights that continued surveillance is required to monitor spread as well as the importance of suppressing the emergence of dually-resistant clones in hospital settings.

Original language	English
Article number	106550
Journal	International Journal of Antimicrobial Agents
Volume	59
Issue number	3
DOIs	https://doi.org/10.1016/j.ijantimicag.2022.106550
Publication status	Published - Mar 2022

Bibliographical note

Funding Information:
This work was supported by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Healthcare Associated Infections and Antimicrobial Resistance at Imperial College London in partnership with Public Health England (PHE) [grant no. HPRU-2012-10047]. EJ is a Rosetrees/Stoneygate 2017 Imperial College Research Fellow, funded by Rosetrees Trust and the Stoneygate Trust [fellowship no. M683]. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health or PHE.

Funding Information:
Uploaded to the ENA under the project number PRJEB23879 and accession numbers ERR3181683, ERR3181601?ERR3181609, ERR3181612?ERR3181614, ERR3181684?ERR3181686, ERR3181688 and ERR3181689. The authors would like to thank Prof. Bruno Gonz?lez-Zorn, Dr Laurent Poirel and Dr Yohei Doi for providing bacterial positive controls for rmtA + rmtE + rmtF, rmtG and rmtH, respectively. The authors would also like to thank staff from the AMRHAI department at Public Health England (PHE) for their assistance with strain characterisation. Finally, the authors would like to thank the Wellcome Trust Sanger Institute for carrying out Illumina sequencing of the bacterial isolates. This work was supported by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Healthcare Associated Infections and Antimicrobial Resistance at Imperial College London in partnership with Public Health England (PHE) [grant no. HPRU-2012-10047]. EJ is a Rosetrees/Stoneygate 2017 Imperial College Research Fellow, funded by Rosetrees Trust and the Stoneygate Trust [fellowship no. M683]. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health or PHE. None declared. Not required.

Publisher Copyright:
© 2022

Keywords

16S RMTase
Aminoglycoside resistance
Carbapenemase
Genetic environment
High-risk clone
Pseudomonas aeruginosa

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1016/j.ijantimicag.2022.106550

Cite this

@article{5909b331f2fa4cf7a6e08ba51ff0c1cc,

title = "Detection and characterisation of 16S rRNA methyltransferase-producing Pseudomonas aeruginosa from the UK and Republic of Ireland from 2003–2015",

abstract = "16S rRNA methyltransferase (16S RMTase) genes confer high-level aminoglycoside resistance, reducing treatment options for multidrug-resistant Gram-negative bacteria. Pseudomonas aeruginosa isolates (n = 221) exhibiting high-level pan-aminoglycoside resistance (amikacin, gentamicin and tobramycin MICs ≥64, ≥32 and ≥32 mg/L, respectively) were screened for 16S RMTase genes to determine their occurrence among isolates submitted to a national reference laboratory from December 2003 to December 2015. 16S RMTase genes were identified using two multiplex PCRs, and whole-genome sequencing (WGS) was used to identify other antibiotic resistance genes, sequence types (STs) and the genetic environment of 16S RMTase genes. 16S RMTase genes were found in 8.6% (19/221) of isolates, with rmtB4 (47.4%; 9/19) being most common, followed by rmtD3 (21.1%; 4/19), rmtF2 (15.8%; 3/19) and single isolates harbouring rmtB1, rmtC and rmtD1. Carbapenemase genes were found in 89.5% (17/19) of 16S RMTase-positive isolates, with blaVIM (52.9%; 9/17) being most common. 16S RMTase genes were found in {\textquoteleft}high-risk{\textquoteright} clones known to harbour carbapenemase genes (ST233, ST277, ST357, ST654 and ST773). Analysis of the genetic environment of 16S RMTase genes identified that IS6100 was genetically linked to rmtB1; IS91 to rmtB4, rmtC or rmtD3; ISCR14 to rmtD1; and rmtF2 was linked to Tn3, IS91 or Tn1721. Although 16S RMTase genes explained only 8.6% of pan-aminoglycoside resistance in the P. aeruginosa isolates studied, the association of 16S RMTase genes with carbapenemase-producers and {\textquoteleft}high-risk{\textquoteright} clones highlights that continued surveillance is required to monitor spread as well as the importance of suppressing the emergence of dually-resistant clones in hospital settings.",

keywords = "16S RMTase, Aminoglycoside resistance, Carbapenemase, Genetic environment, High-risk clone, Pseudomonas aeruginosa",

author = "Emma Taylor and Elita Jauneikaite and Shiranee Sriskandan and Neil Woodford and Hopkins, {Katie L.}",

note = "Funding Information: This work was supported by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Healthcare Associated Infections and Antimicrobial Resistance at Imperial College London in partnership with Public Health England (PHE) [grant no. HPRU-2012-10047]. EJ is a Rosetrees/Stoneygate 2017 Imperial College Research Fellow, funded by Rosetrees Trust and the Stoneygate Trust [fellowship no. M683]. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health or PHE. Funding Information: Uploaded to the ENA under the project number PRJEB23879 and accession numbers ERR3181683, ERR3181601?ERR3181609, ERR3181612?ERR3181614, ERR3181684?ERR3181686, ERR3181688 and ERR3181689. The authors would like to thank Prof. Bruno Gonz?lez-Zorn, Dr Laurent Poirel and Dr Yohei Doi for providing bacterial positive controls for rmtA + rmtE + rmtF, rmtG and rmtH, respectively. The authors would also like to thank staff from the AMRHAI department at Public Health England (PHE) for their assistance with strain characterisation. Finally, the authors would like to thank the Wellcome Trust Sanger Institute for carrying out Illumina sequencing of the bacterial isolates. This work was supported by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Healthcare Associated Infections and Antimicrobial Resistance at Imperial College London in partnership with Public Health England (PHE) [grant no. HPRU-2012-10047]. EJ is a Rosetrees/Stoneygate 2017 Imperial College Research Fellow, funded by Rosetrees Trust and the Stoneygate Trust [fellowship no. M683]. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health or PHE. None declared. Not required. Publisher Copyright: {\textcopyright} 2022",

year = "2022",

month = mar,

doi = "10.1016/j.ijantimicag.2022.106550",

language = "English",

volume = "59",

journal = "International Journal of Antimicrobial Agents",

issn = "0924-8579",

publisher = "Elsevier",

number = "3",

}

TY - JOUR

T1 - Detection and characterisation of 16S rRNA methyltransferase-producing Pseudomonas aeruginosa from the UK and Republic of Ireland from 2003–2015

AU - Taylor, Emma

AU - Jauneikaite, Elita

AU - Sriskandan, Shiranee

AU - Woodford, Neil

AU - Hopkins, Katie L.

N1 - Funding Information: This work was supported by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Healthcare Associated Infections and Antimicrobial Resistance at Imperial College London in partnership with Public Health England (PHE) [grant no. HPRU-2012-10047]. EJ is a Rosetrees/Stoneygate 2017 Imperial College Research Fellow, funded by Rosetrees Trust and the Stoneygate Trust [fellowship no. M683]. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health or PHE. Funding Information: Uploaded to the ENA under the project number PRJEB23879 and accession numbers ERR3181683, ERR3181601?ERR3181609, ERR3181612?ERR3181614, ERR3181684?ERR3181686, ERR3181688 and ERR3181689. The authors would like to thank Prof. Bruno Gonz?lez-Zorn, Dr Laurent Poirel and Dr Yohei Doi for providing bacterial positive controls for rmtA + rmtE + rmtF, rmtG and rmtH, respectively. The authors would also like to thank staff from the AMRHAI department at Public Health England (PHE) for their assistance with strain characterisation. Finally, the authors would like to thank the Wellcome Trust Sanger Institute for carrying out Illumina sequencing of the bacterial isolates. This work was supported by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Healthcare Associated Infections and Antimicrobial Resistance at Imperial College London in partnership with Public Health England (PHE) [grant no. HPRU-2012-10047]. EJ is a Rosetrees/Stoneygate 2017 Imperial College Research Fellow, funded by Rosetrees Trust and the Stoneygate Trust [fellowship no. M683]. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health or PHE. None declared. Not required. Publisher Copyright: © 2022

PY - 2022/3

Y1 - 2022/3

N2 - 16S rRNA methyltransferase (16S RMTase) genes confer high-level aminoglycoside resistance, reducing treatment options for multidrug-resistant Gram-negative bacteria. Pseudomonas aeruginosa isolates (n = 221) exhibiting high-level pan-aminoglycoside resistance (amikacin, gentamicin and tobramycin MICs ≥64, ≥32 and ≥32 mg/L, respectively) were screened for 16S RMTase genes to determine their occurrence among isolates submitted to a national reference laboratory from December 2003 to December 2015. 16S RMTase genes were identified using two multiplex PCRs, and whole-genome sequencing (WGS) was used to identify other antibiotic resistance genes, sequence types (STs) and the genetic environment of 16S RMTase genes. 16S RMTase genes were found in 8.6% (19/221) of isolates, with rmtB4 (47.4%; 9/19) being most common, followed by rmtD3 (21.1%; 4/19), rmtF2 (15.8%; 3/19) and single isolates harbouring rmtB1, rmtC and rmtD1. Carbapenemase genes were found in 89.5% (17/19) of 16S RMTase-positive isolates, with blaVIM (52.9%; 9/17) being most common. 16S RMTase genes were found in ‘high-risk’ clones known to harbour carbapenemase genes (ST233, ST277, ST357, ST654 and ST773). Analysis of the genetic environment of 16S RMTase genes identified that IS6100 was genetically linked to rmtB1; IS91 to rmtB4, rmtC or rmtD3; ISCR14 to rmtD1; and rmtF2 was linked to Tn3, IS91 or Tn1721. Although 16S RMTase genes explained only 8.6% of pan-aminoglycoside resistance in the P. aeruginosa isolates studied, the association of 16S RMTase genes with carbapenemase-producers and ‘high-risk’ clones highlights that continued surveillance is required to monitor spread as well as the importance of suppressing the emergence of dually-resistant clones in hospital settings.

AB - 16S rRNA methyltransferase (16S RMTase) genes confer high-level aminoglycoside resistance, reducing treatment options for multidrug-resistant Gram-negative bacteria. Pseudomonas aeruginosa isolates (n = 221) exhibiting high-level pan-aminoglycoside resistance (amikacin, gentamicin and tobramycin MICs ≥64, ≥32 and ≥32 mg/L, respectively) were screened for 16S RMTase genes to determine their occurrence among isolates submitted to a national reference laboratory from December 2003 to December 2015. 16S RMTase genes were identified using two multiplex PCRs, and whole-genome sequencing (WGS) was used to identify other antibiotic resistance genes, sequence types (STs) and the genetic environment of 16S RMTase genes. 16S RMTase genes were found in 8.6% (19/221) of isolates, with rmtB4 (47.4%; 9/19) being most common, followed by rmtD3 (21.1%; 4/19), rmtF2 (15.8%; 3/19) and single isolates harbouring rmtB1, rmtC and rmtD1. Carbapenemase genes were found in 89.5% (17/19) of 16S RMTase-positive isolates, with blaVIM (52.9%; 9/17) being most common. 16S RMTase genes were found in ‘high-risk’ clones known to harbour carbapenemase genes (ST233, ST277, ST357, ST654 and ST773). Analysis of the genetic environment of 16S RMTase genes identified that IS6100 was genetically linked to rmtB1; IS91 to rmtB4, rmtC or rmtD3; ISCR14 to rmtD1; and rmtF2 was linked to Tn3, IS91 or Tn1721. Although 16S RMTase genes explained only 8.6% of pan-aminoglycoside resistance in the P. aeruginosa isolates studied, the association of 16S RMTase genes with carbapenemase-producers and ‘high-risk’ clones highlights that continued surveillance is required to monitor spread as well as the importance of suppressing the emergence of dually-resistant clones in hospital settings.

KW - 16S RMTase

KW - Aminoglycoside resistance

KW - Carbapenemase

KW - Genetic environment

KW - High-risk clone

KW - Pseudomonas aeruginosa

UR - http://www.scopus.com/inward/record.url?scp=85125360521&partnerID=8YFLogxK

U2 - 10.1016/j.ijantimicag.2022.106550

DO - 10.1016/j.ijantimicag.2022.106550

M3 - Article

C2 - 35176475

AN - SCOPUS:85125360521

SN - 0924-8579

VL - 59

JO - International Journal of Antimicrobial Agents

JF - International Journal of Antimicrobial Agents

IS - 3

M1 - 106550

ER -

Detection and characterisation of 16S rRNA methyltransferase-producing Pseudomonas aeruginosa from the UK and Republic of Ireland from 2003–2015

Abstract

Bibliographical note

Keywords

UN SDGs

Access to Document

Other files and links

Fingerprint

Cite this