Sentinel Surveillance Reveals Emerging Daptomycin-Resistant ST736 Enterococcus faecium and Multiple Mechanisms of Linezolid Resistance in Enterococci in the United States

Enterococcus faecalis and faecium with resistance to daptomycin and/or linezolid are emerging globally. We present the genomic characterization of daptomycin- and linezolid-resistant E. faecalis and E. faecium surveillance isolates from the United States, 2013–2016. Daptomycin resistance was low amo...

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Main Authors: Amy S. Gargis, Lori M. Spicer, Alyssa G. Kent, Wenming Zhu, Davina Campbell, Gillian McAllister, Thomas O. Ewing, Valerie Albrecht, Valerie A. Stevens, Mili Sheth, Jasmine Padilla, Dhwani Batra, J. Kristie Johnson, Alison Laufer Halpin, J. Kamile Rasheed, Christopher A. Elkins, Maria Karlsson, Joseph D. Lutgring
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.807398/full
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author Amy S. Gargis
Lori M. Spicer
Lori M. Spicer
Alyssa G. Kent
Alyssa G. Kent
Wenming Zhu
Davina Campbell
Gillian McAllister
Thomas O. Ewing
Thomas O. Ewing
Valerie Albrecht
Valerie A. Stevens
Mili Sheth
Jasmine Padilla
Jasmine Padilla
Dhwani Batra
J. Kristie Johnson
Alison Laufer Halpin
J. Kamile Rasheed
Christopher A. Elkins
Maria Karlsson
Joseph D. Lutgring
author_facet Amy S. Gargis
Lori M. Spicer
Lori M. Spicer
Alyssa G. Kent
Alyssa G. Kent
Wenming Zhu
Davina Campbell
Gillian McAllister
Thomas O. Ewing
Thomas O. Ewing
Valerie Albrecht
Valerie A. Stevens
Mili Sheth
Jasmine Padilla
Jasmine Padilla
Dhwani Batra
J. Kristie Johnson
Alison Laufer Halpin
J. Kamile Rasheed
Christopher A. Elkins
Maria Karlsson
Joseph D. Lutgring
author_sort Amy S. Gargis
collection DOAJ
description Enterococcus faecalis and faecium with resistance to daptomycin and/or linezolid are emerging globally. We present the genomic characterization of daptomycin- and linezolid-resistant E. faecalis and E. faecium surveillance isolates from the United States, 2013–2016. Daptomycin resistance was low among E. faecalis (2/364, 0.5%) and E. faecium (17/344, 5%). The majority (71%, 12/17) of daptomycin-resistant E. faecium isolates belonged to the emerging ST736 clone and contained mutations in liaFSR and cls previously associated with resistance. However, 1/2 E. faecalis and 3/17 E. faecium did not contain these mutations previously associated with daptomycin resistance. Linezolid resistance was rare among E. faecalis (1/364, 0.3%) and E. faecium (2/344, 0.6%). These two E. faecium isolates, one of which was also resistant to daptomycin and vancomycin, contained the 23S rRNA nucleotide mutation (G2576T) associated with linezolid resistance. Long-read sequencing revealed the linezolid-resistant E. faecalis isolate contained chromosomal- and plasmid-encoded copies of optrA. The chromosomal optrA was located on the recently described Tn6674 multiresistance transposon. The second copy of optrA was encoded on an ∼65 kb mosaic plasmid, with component regions sharing high sequence identity to optrA-encoding multiresistance plasmids of animal origin. The optrA-encoding plasmid contained open reading frames predicted to encode proteins associated with a pheromone-responsive plasmid transfer system, and filter mating experiments confirmed the plasmid was conjugative. Continued surveillance of enterococci is necessary to assess the prevalence and trends of daptomycin and linezolid resistance in the United States, characterize resistance mechanisms and how they transfer, and monitor for emerging sequence types associated with resistance.
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spelling doaj.art-cc3dc2ad36be4fdbab97f3c7c81f9e432022-12-21T20:21:51ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-02-011210.3389/fmicb.2021.807398807398Sentinel Surveillance Reveals Emerging Daptomycin-Resistant ST736 Enterococcus faecium and Multiple Mechanisms of Linezolid Resistance in Enterococci in the United StatesAmy S. Gargis0Lori M. Spicer1Lori M. Spicer2Alyssa G. Kent3Alyssa G. Kent4Wenming Zhu5Davina Campbell6Gillian McAllister7Thomas O. Ewing8Thomas O. Ewing9Valerie Albrecht10Valerie A. Stevens11Mili Sheth12Jasmine Padilla13Jasmine Padilla14Dhwani Batra15J. Kristie Johnson16Alison Laufer Halpin17J. Kamile Rasheed18Christopher A. Elkins19Maria Karlsson20Joseph D. Lutgring21Division of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesGoldbelt C6, LLC, Chesapeake, VA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesGoldbelt C6, LLC, Chesapeake, VA, United StatesDivision of Tuberculosis Elimination, National Center for HIV/AIDS, Viral Hepatitis, STD and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesGoldbelt C6, LLC, Chesapeake, VA, United StatesOffice of the Director, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesBiotechnology Core Facility Branch, Division of Scientific Resources, Centers for Disease Control and Prevention, Atlanta, GA, United StatesBiotechnology Core Facility Branch, Division of Scientific Resources, Centers for Disease Control and Prevention, Atlanta, GA, United StatesASRT Incorporated, Atlanta, GA, United StatesBiotechnology Core Facility Branch, Division of Scientific Resources, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDepartment of Pathology, University of Maryland School of Medicine, Baltimore, MD, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesDivision of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United StatesEnterococcus faecalis and faecium with resistance to daptomycin and/or linezolid are emerging globally. We present the genomic characterization of daptomycin- and linezolid-resistant E. faecalis and E. faecium surveillance isolates from the United States, 2013–2016. Daptomycin resistance was low among E. faecalis (2/364, 0.5%) and E. faecium (17/344, 5%). The majority (71%, 12/17) of daptomycin-resistant E. faecium isolates belonged to the emerging ST736 clone and contained mutations in liaFSR and cls previously associated with resistance. However, 1/2 E. faecalis and 3/17 E. faecium did not contain these mutations previously associated with daptomycin resistance. Linezolid resistance was rare among E. faecalis (1/364, 0.3%) and E. faecium (2/344, 0.6%). These two E. faecium isolates, one of which was also resistant to daptomycin and vancomycin, contained the 23S rRNA nucleotide mutation (G2576T) associated with linezolid resistance. Long-read sequencing revealed the linezolid-resistant E. faecalis isolate contained chromosomal- and plasmid-encoded copies of optrA. The chromosomal optrA was located on the recently described Tn6674 multiresistance transposon. The second copy of optrA was encoded on an ∼65 kb mosaic plasmid, with component regions sharing high sequence identity to optrA-encoding multiresistance plasmids of animal origin. The optrA-encoding plasmid contained open reading frames predicted to encode proteins associated with a pheromone-responsive plasmid transfer system, and filter mating experiments confirmed the plasmid was conjugative. Continued surveillance of enterococci is necessary to assess the prevalence and trends of daptomycin and linezolid resistance in the United States, characterize resistance mechanisms and how they transfer, and monitor for emerging sequence types associated with resistance.https://www.frontiersin.org/articles/10.3389/fmicb.2021.807398/fullEnterococcus faecalisEnterococcus faeciumdaptomycinlinezolidconjugationoptrA
spellingShingle Amy S. Gargis
Lori M. Spicer
Lori M. Spicer
Alyssa G. Kent
Alyssa G. Kent
Wenming Zhu
Davina Campbell
Gillian McAllister
Thomas O. Ewing
Thomas O. Ewing
Valerie Albrecht
Valerie A. Stevens
Mili Sheth
Jasmine Padilla
Jasmine Padilla
Dhwani Batra
J. Kristie Johnson
Alison Laufer Halpin
J. Kamile Rasheed
Christopher A. Elkins
Maria Karlsson
Joseph D. Lutgring
Sentinel Surveillance Reveals Emerging Daptomycin-Resistant ST736 Enterococcus faecium and Multiple Mechanisms of Linezolid Resistance in Enterococci in the United States
Frontiers in Microbiology
Enterococcus faecalis
Enterococcus faecium
daptomycin
linezolid
conjugation
optrA
title Sentinel Surveillance Reveals Emerging Daptomycin-Resistant ST736 Enterococcus faecium and Multiple Mechanisms of Linezolid Resistance in Enterococci in the United States
title_full Sentinel Surveillance Reveals Emerging Daptomycin-Resistant ST736 Enterococcus faecium and Multiple Mechanisms of Linezolid Resistance in Enterococci in the United States
title_fullStr Sentinel Surveillance Reveals Emerging Daptomycin-Resistant ST736 Enterococcus faecium and Multiple Mechanisms of Linezolid Resistance in Enterococci in the United States
title_full_unstemmed Sentinel Surveillance Reveals Emerging Daptomycin-Resistant ST736 Enterococcus faecium and Multiple Mechanisms of Linezolid Resistance in Enterococci in the United States
title_short Sentinel Surveillance Reveals Emerging Daptomycin-Resistant ST736 Enterococcus faecium and Multiple Mechanisms of Linezolid Resistance in Enterococci in the United States
title_sort sentinel surveillance reveals emerging daptomycin resistant st736 enterococcus faecium and multiple mechanisms of linezolid resistance in enterococci in the united states
topic Enterococcus faecalis
Enterococcus faecium
daptomycin
linezolid
conjugation
optrA
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.807398/full
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