Genetic characterization of three qnrS1-harbouring multidrug-resistance plasmids and qnrS1-containing transposons circulating in Ho Chi Minh City, Vietnam
Plasmid-mediated quinolone resistance (PMQR) refers to a family of closely related genes that confer decreased susceptibility to fluoroquinolones. PMQR genes are generally associated with integrons and/or plasmids that carry additional antimicrobial resistance genes active against a range of antimic...
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Published in | Journal of medical microbiology Vol. 64; no. 8; pp. 869 - 878 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Society for General Microbiology
01.08.2015
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Abstract | Plasmid-mediated quinolone resistance (PMQR) refers to a family of closely related genes that confer decreased susceptibility to fluoroquinolones. PMQR genes are generally associated with integrons and/or plasmids that carry additional antimicrobial resistance genes active against a range of antimicrobials. In Ho Chi Minh City (HCMC), Vietnam, we have previously shown a high frequency of PMQR genes within commensal Enterobacteriaceae. However, there are limited available sequence data detailing the genetic context in which the PMQR genes reside, and a lack of understanding of how these genes spread across the Enterobacteriaceae. Here, we aimed to determine the genetic background facilitating the spread and maintenance of qnrS1, the dominant PMQR gene circulating in HCMC. We sequenced three qnrS1-carrying plasmids in their entirety to understand the genetic context of these qnrS1-embedded plasmids and also the association of qnrS1-mediated quinolone resistance with other antimicrobial resistance phenotypes. Annotation of the three qnrS1-containing plasmids revealed a qnrS1-containing transposon with a closely related structure. We screened 112 qnrS1-positive commensal Enterobacteriaceae isolated in the community and in a hospital in HCMC to detect the common transposon structure. We found the same transposon structure to be present in 71.4 % (45/63) of qnrS1-positive hospital isolates and in 36.7 % (18/49) of qnrS1-positive isolates from the community. The resulting sequence analysis of the qnrS1 environment suggested that qnrS1 genes are widely distributed and are mobilized on elements with a common genetic background. Our data add additional insight into mechanisms that facilitate resistance to multiple antimicrobials in Gram-negative bacteria in Vietnam. |
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AbstractList | Plasmid-mediated quinolone resistance (PMQR) refers to a family of closely related genes that confer decreased susceptibility to fluoroquinolones. PMQR genes are generally associated with integrons and/or plasmids that carry additional antimicrobial resistance genes active against a range of antimicrobials. In Ho Chi Minh City (HCMC), Vietnam, we have previously shown a high frequency of PMQR genes within commensal
Enterobacteriaceae
. However, there are limited available sequence data detailing the genetic context in which the PMQR genes reside, and a lack of understanding of how these genes spread across the
Enterobacteriaceae
. Here, we aimed to determine the genetic background facilitating the spread and maintenance of
qnrS1,
the dominant PMQR gene circulating in HCMC. We sequenced three
qnrS1
-carrying plasmids in their entirety to understand the genetic context of these
qnrS1
-embedded plasmids and also the association of
qnrS1
-mediated quinolone resistance with other antimicrobial resistance phenotypes. Annotation of the three
qnrS1
-containing plasmids revealed a
qnrS1
-containing transposon with a closely related structure. We screened 112
qnrS1
-positive commensal
Enterobacteriaceae
isolated in the community and in a hospital in HCMC to detect the common transposon structure. We found the same transposon structure to be present in 71.4 % (45/63) of
qnrS1
-positive hospital isolates and in 36.7 % (18/49) of
qnrS1
-positive isolates from the community. The resulting sequence analysis of the
qnrS1
environment suggested that
qnrS1
genes are widely distributed and are mobilized on elements with a common genetic background. Our data add additional insight into mechanisms that facilitate resistance to multiple antimicrobials in Gram-negative bacteria in Vietnam. Plasmid-mediated quinolone resistance (PMQR) refers to a family of closely related genes that confer decreased susceptibility to fluoroquinolones. PMQR genes are generally associated with integrons and/or plasmids that carry additional antimicrobial resistance genes active against a range of antimicrobials. In Ho Chi Minh City (HCMC), Vietnam, we have previously shown a high frequency of PMQR genes within commensal Enterobacteriaceae. However, there are limited available sequence data detailing the genetic context in which the PMQR genes reside, and a lack of understanding of how these genes spread across the Enterobacteriaceae. Here, we aimed to determine the genetic background facilitating the spread and maintenance of qnrS1, the dominant PMQR gene circulating in HCMC. We sequenced three qnrS1-carrying plasmids in their entirety to understand the genetic context of these qnrS1-embedded plasmids and also the association of qnrS1-mediated quinolone resistance with other antimicrobial resistance phenotypes. Annotation of the three qnrS1-containing plasmids revealed a qnrS1-containing transposon with a closely related structure. We screened 112 qnrS1-positive commensal Enterobacteriaceae isolated in the community and in a hospital in HCMC to detect the common transposon structure. We found the same transposon structure to be present in 71.4 % (45/63) of qnrS1-positive hospital isolates and in 36.7 % (18/49) of qnrS1-positive isolates from the community. The resulting sequence analysis of the qnrS1 environment suggested that qnrS1 genes are widely distributed and are mobilized on elements with a common genetic background. Our data add additional insight into mechanisms that facilitate resistance to multiple antimicrobials in Gram-negative bacteria in Vietnam. |
Author | Nhu, Tran Do Hoang Thwaites, Guy Campbell, James I Tam, Pham Thi Thanh Le, Vien Nhu, Nguyen Thi Khanh Thomson, Nicholas R Tuyen, Ha Thanh Cerdeno-Tarraga, Ana Baker, Stephen Schultsz, Constance |
Author_xml | – sequence: 1 givenname: Vien surname: Le fullname: Le, Vien organization: Division of Infectious Diseases, Department of Medicine, University of California, San Francisco, CA, USA – sequence: 2 givenname: Nguyen Thi Khanh surname: Nhu fullname: Nhu, Nguyen Thi Khanh organization: School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, Australia – sequence: 3 givenname: Ana surname: Cerdeno-Tarraga fullname: Cerdeno-Tarraga, Ana organization: EMBL-European Bioinformatics Institute, Hinxton, Cambridge, UK – sequence: 4 givenname: James I surname: Campbell fullname: Campbell, James I organization: Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, Oxford University, UK – sequence: 5 givenname: Ha Thanh surname: Tuyen fullname: Tuyen, Ha Thanh organization: Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam – sequence: 6 givenname: Tran Do Hoang surname: Nhu fullname: Nhu, Tran Do Hoang organization: Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam – sequence: 7 givenname: Pham Thi Thanh surname: Tam fullname: Tam, Pham Thi Thanh organization: Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam – sequence: 8 givenname: Constance surname: Schultsz fullname: Schultsz, Constance organization: Department of Medical Microbiology, Academic Medical Centre, University of Amsterdam, The Netherlands – sequence: 9 givenname: Guy surname: Thwaites fullname: Thwaites, Guy organization: Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, Oxford University, UK – sequence: 10 givenname: Nicholas R surname: Thomson fullname: Thomson, Nicholas R organization: London School of Hygiene and Tropical Medicine, London, UK – sequence: 11 givenname: Stephen surname: Baker fullname: Baker, Stephen organization: London School of Hygiene and Tropical Medicine, London, UK |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The GenBank/EMBL/DDBJ accession numbers for the sequences determined in this study are HF545433 (pE66An), HF545435 (pK18An) and HF545434 (pK1HV). |
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References | jmm000100-Carattoli1 jmm000100-Kehrenberg1 jmm000100-Huang1 Vien (jmm000100-Vien1) 2009; 58 jmm000100-Chung1 Kado (jmm000100-Kado1) 1981; 145 jmm000100-Lodwick1 jmm000100-Kehrenberg12 jmm000100-Carver12 jmm000100-Sundin1 jmm000100-Gestal1 jmm000100-Wang1 jmm000100-Kim1 jmm000100-Carver1 jmm000100-Som1 jmm000100-Chen1 jmm000100-Wu1 jmm000100-Castanheira1 Park (jmm000100-Park1) 2009; 39 jmm000100-Parkhill1 jmm000100-Nga1 jmm000100-Poirel1 jmm000100-Cavaco1 jmm000100-Zhao1 jmm000100-Hamouda1 jmm000100-Hochhut1 jmm000100-Bou1 jmm000100-Vien12 jmm000100-Dobiasova1 jmm000100-Jacoby1 jmm000100-Holt1 jmm000100-Strahilevitz1 jmm000100-Hata1 jmm000100-Garnier1 jmm000100-Tran1 jmm000100-Rutherford1 jmm000100-Sumrall1 jmm000100-Cao1 jmm000100-Dahmen1 jmm000100-Lavigne1 jmm000100-Hu1 jmm000100-Martinez-Martinez1 jmm000100-Literak1 jmm000100-Nhu1 jmm000100-Fricke1 jmm000100-Beliaev1 jmm000100-Poirel12 jmm000100-Kobayashi1 jmm000100-Vien123 Bhagwat (jmm000100-Bhagwat1) 1990; 265 jmm000100-Cano1 |
References_xml | – ident: jmm000100-Garnier1 doi: 10.1128/AAC.00293-06 – ident: jmm000100-Literak1 doi: 10.1128/AEM.01446-10 – ident: jmm000100-Hata1 doi: 10.1128/AAC.49.2.801-803.2005 – ident: jmm000100-Wu1 doi: 10.1093/jac/dkn426 – ident: jmm000100-Gestal1 doi: 10.1128/AAC.49.11.4771-4774.2005 – ident: jmm000100-Kehrenberg1 doi: 10.1093/jac/dkl213 – ident: jmm000100-Carattoli1 doi: 10.1093/jac/dkq269 – ident: jmm000100-Lodwick1 doi: 10.1093/nar/18.17.5045 – ident: jmm000100-Dahmen1 doi: 10.1111/j.1469-0691.2009.03010.x – ident: jmm000100-Strahilevitz1 doi: 10.1128/CMR.00016-09 – ident: jmm000100-Sundin1 doi: 10.1111/j.1365-294X.1996.tb00299.x – ident: jmm000100-Hamouda1 doi: 10.1179/joc.2008.20.6.753 – ident: jmm000100-Poirel1 doi: 10.1128/AAC.00597-06 – volume: 145 start-page: 1365 year: 1981 ident: jmm000100-Kado1 article-title: Rapid procedure for detection and isolation of large and small plasmids publication-title: J Bacteriol doi: 10.1128/jb.145.3.1365-1373.1981 contributor: fullname: Kado – ident: jmm000100-Kobayashi1 doi: 10.1093/nar/29.18.3742 – ident: jmm000100-Dobiasova1 doi: 10.1111/1574-6941.12149 – ident: jmm000100-Sumrall1 doi: 10.1371/journal.pone.0110279 – ident: jmm000100-Chen1 doi: 10.1128/AAC.00456-06 – ident: jmm000100-Huang1 doi: 10.1016/j.jhin.2008.04.012 – ident: jmm000100-Fricke1 doi: 10.1128/JB.00189-09 – ident: jmm000100-Tran1 doi: 10.1371/journal.pone.0011778 – volume: 39 start-page: 55 year: 2009 ident: jmm000100-Park1 article-title: Accumulation of plasmid-mediated fluoroquinolone resistance genes, qepA qnrS1, in Enterobacter aerogenes co-producing RmtB and class A β-lactamase LAP-1 publication-title: Ann Clin Lab Sci contributor: fullname: Park – ident: jmm000100-Hu1 doi: 10.1111/j.1745-7254.2008.00757.x – ident: jmm000100-Castanheira1 doi: 10.1128/AAC.00780-06 – ident: jmm000100-Rutherford1 doi: 10.1093/bioinformatics/16.10.944 – ident: jmm000100-Nga1 doi: 10.1016/j.trstmh.2011.10.004 – volume: 58 start-page: 1585 year: 2009 ident: jmm000100-Vien1 article-title: High prevalence of plasmid-mediated quinolone resistance determinants in commensal members of the Enterobacteriaceae in Ho Chi Minh City, Vietnam publication-title: J Med Microbiol doi: 10.1099/jmm.0.010033-0 contributor: fullname: Vien – volume: 265 start-page: 767 year: 1990 ident: jmm000100-Bhagwat1 article-title: Primary sequence of the EcoRII endonuclease and properties of its fusions with β-galactosidase publication-title: J Biol Chem doi: 10.1016/S0021-9258(19)40116-6 contributor: fullname: Bhagwat – ident: jmm000100-Jacoby1 doi: 10.1128/AAC.50.4.1178-1182.2006 – ident: jmm000100-Carver1 doi: 10.1093/bioinformatics/btn529 – ident: jmm000100-Zhao1 doi: 10.1371/journal.pone.0010141 – ident: jmm000100-Kim1 doi: 10.1111/j.1348-0421.1994.tb01741.x – ident: jmm000100-Vien123 doi: 10.1371/journal.pone.0042919 – ident: jmm000100-Kehrenberg12 doi: 10.1093/jac/dkm283 – ident: jmm000100-Poirel12 doi: 10.1128/AAC.01082-06 – ident: jmm000100-Parkhill1 doi: 10.1038/35097083 – ident: jmm000100-Martinez-Martinez1 doi: 10.1016/S0140-6736(97)07322-4 – ident: jmm000100-Holt1 doi: 10.1073/pnas.1308632110 – ident: jmm000100-Wang1 doi: 10.1128/AAC.01400-08 – ident: jmm000100-Cao1 doi: 10.1128/AAC.46.5.1212-1217.2002 – ident: jmm000100-Nhu1 doi: 10.1099/jmm.0.076646-0 – ident: jmm000100-Bou1 doi: 10.1128/JCM.40.11.4030-4036.2002 – ident: jmm000100-Carver12 doi: 10.1093/bioinformatics/btn578 – ident: jmm000100-Cavaco1 doi: 10.1128/AAC.00997-08 – ident: jmm000100-Vien12 doi: 10.1128/AAC.01200-10 – ident: jmm000100-Hochhut1 doi: 10.1111/j.1365-2958.2006.05255.x – ident: jmm000100-Som1 doi: 10.1093/nar/15.1.313 – ident: jmm000100-Beliaev1 doi: 10.1128/JB.184.16.4612-4616.2002 – ident: jmm000100-Chung1 doi: 10.15252/emmm.201404767 – ident: jmm000100-Cano1 doi: 10.1128/JCM.02229-08 – ident: jmm000100-Lavigne1 doi: 10.1128/AAC.00904-06 |
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Snippet | Plasmid-mediated quinolone resistance (PMQR) refers to a family of closely related genes that confer decreased susceptibility to fluoroquinolones. PMQR genes... |
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SubjectTerms | Anti-Bacterial Agents - pharmacology Community-Acquired Infections - microbiology Cross Infection - microbiology DNA Transposable Elements DNA, Bacterial - chemistry DNA, Bacterial - genetics Drug Resistance, Multiple, Bacterial Enterobacteriaceae - drug effects Enterobacteriaceae - genetics Enterobacteriaceae - isolation & purification Enterobacteriaceae Infections - microbiology Humans Interspersed Repetitive Sequences Molecular Sequence Data Plasmids Quinolones - pharmacology Sequence Analysis, DNA Vietnam |
Title | Genetic characterization of three qnrS1-harbouring multidrug-resistance plasmids and qnrS1-containing transposons circulating in Ho Chi Minh City, Vietnam |
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