Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution

Background Multidrug-resistant Neisseria gonorrhoeae strains are prevalent, threatening gonorrhoea treatment globally, and understanding of emergence, evolution, and spread of antimicrobial resistance (AMR) in gonococci remains limited. We describe the genomic evolution of gonococci and their AMR, r...

Descripción completa

Detalles Bibliográficos
Autores: Golparian, D, Harris, SR, Sanchez-Buso, L, Hoffmann, S, Shafer, WM, Bentley, SD, Jensen, JS, Unemo, M
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Institución:Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)
Repositorio:r-FISABIO. Repositorio Institucional de Producción Científica
OAI Identifier:oai:fisabio.fundanetsuite.com:p15231
Acceso en línea:https://fisabio.portalinvestigacion.com/publicaciones/15231
Access Level:acceso abierto
Palabra clave:Neisseria gonorrhoeae
Antimicrobial resistance
Evolution
Whole-genome sequencing
Genomic epidemiology
Temporal analysis
id ES_05e4e67efbdd6c4fd2ee121d9418ed69
oai_identifier_str oai:fisabio.fundanetsuite.com:p15231
network_acronym_str ES
network_name_str España
repository_id_str
spelling Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolutionGolparian, DHarris, SRSanchez-Buso, LHoffmann, SShafer, WMBentley, SDJensen, JSUnemo, MNeisseria gonorrhoeaeAntimicrobial resistanceEvolutionWhole-genome sequencingGenomic epidemiologyTemporal analysisBackground Multidrug-resistant Neisseria gonorrhoeae strains are prevalent, threatening gonorrhoea treatment globally, and understanding of emergence, evolution, and spread of antimicrobial resistance (AMR) in gonococci remains limited. We describe the genomic evolution of gonococci and their AMR, related to the introduction of antimicrobial therapies, examining isolates from 1928 (preantibiotic era) to 2013 in Denmark. This is, to our knowledge, the oldest gonococcal collection globally. Methods Lyophilised isolates were revived and examined using Etest (18 antimicrobials) and whole-genome sequencing (WGS). Quality-assured genome sequences were obtained for 191 viable and 40 non-viable isolates and analysed with multiple phylogenomic approaches. Results Gonococcal AMR, including an accumulation of multiple AMR determinants, started to emerge particularly in the 1950s-1970s. By the twenty-first century, resistance to most antimicrobials was common. Despite that some AMR determinants affect many physiological functions and fitness, AMR determinants were mainly selected by the use/misuse of gonorrhoea therapeutic antimicrobials. Most AMR developed in strains belonging to one multidrug-resistant (MDR) clade with close to three times higher genomic mutation rate. Modern N. gonorrhoeae was inferred to have emerged in the late-1500s and its genome became increasingly conserved over time. Conclusions WGS of gonococci from 1928 to 2013 showed that no AMR determinants, except penB, were in detectable frequency before the introduction of gonorrhoea therapeutic antimicrobials. The modern gonococcus is substantially younger than previously hypothesized and has been evolving into a more clonal species, driven by the use/misuse of antimicrobials. The MDR gonococcal clade should be further investigated for early detection of strains with predispositions to develop and maintain MDR and for initiation of public health interventions.BMC2020info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttps://fisabio.portalinvestigacion.com/publicaciones/15231BMC GENOMICSISSN: 14712164reponame:r-FISABIO. Repositorio Institucional de Producción Científicainstname:Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)Inglésinfo:eu-repo/semantics/openAccessoai:fisabio.fundanetsuite.com:p152312026-06-11T12:45:17Z
dc.title.none.fl_str_mv Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution
title Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution
spellingShingle Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution
Golparian, D
Neisseria gonorrhoeae
Antimicrobial resistance
Evolution
Whole-genome sequencing
Genomic epidemiology
Temporal analysis
title_short Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution
title_full Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution
title_fullStr Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution
title_full_unstemmed Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution
title_sort Genomic evolution of <i>Neisseria gonorrhoeae</i> since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution
dc.creator.none.fl_str_mv Golparian, D
Harris, SR
Sanchez-Buso, L
Hoffmann, S
Shafer, WM
Bentley, SD
Jensen, JS
Unemo, M
author Golparian, D
author_facet Golparian, D
Harris, SR
Sanchez-Buso, L
Hoffmann, S
Shafer, WM
Bentley, SD
Jensen, JS
Unemo, M
author_role author
author2 Harris, SR
Sanchez-Buso, L
Hoffmann, S
Shafer, WM
Bentley, SD
Jensen, JS
Unemo, M
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Neisseria gonorrhoeae
Antimicrobial resistance
Evolution
Whole-genome sequencing
Genomic epidemiology
Temporal analysis
topic Neisseria gonorrhoeae
Antimicrobial resistance
Evolution
Whole-genome sequencing
Genomic epidemiology
Temporal analysis
description Background Multidrug-resistant Neisseria gonorrhoeae strains are prevalent, threatening gonorrhoea treatment globally, and understanding of emergence, evolution, and spread of antimicrobial resistance (AMR) in gonococci remains limited. We describe the genomic evolution of gonococci and their AMR, related to the introduction of antimicrobial therapies, examining isolates from 1928 (preantibiotic era) to 2013 in Denmark. This is, to our knowledge, the oldest gonococcal collection globally. Methods Lyophilised isolates were revived and examined using Etest (18 antimicrobials) and whole-genome sequencing (WGS). Quality-assured genome sequences were obtained for 191 viable and 40 non-viable isolates and analysed with multiple phylogenomic approaches. Results Gonococcal AMR, including an accumulation of multiple AMR determinants, started to emerge particularly in the 1950s-1970s. By the twenty-first century, resistance to most antimicrobials was common. Despite that some AMR determinants affect many physiological functions and fitness, AMR determinants were mainly selected by the use/misuse of gonorrhoea therapeutic antimicrobials. Most AMR developed in strains belonging to one multidrug-resistant (MDR) clade with close to three times higher genomic mutation rate. Modern N. gonorrhoeae was inferred to have emerged in the late-1500s and its genome became increasingly conserved over time. Conclusions WGS of gonococci from 1928 to 2013 showed that no AMR determinants, except penB, were in detectable frequency before the introduction of gonorrhoea therapeutic antimicrobials. The modern gonococcus is substantially younger than previously hypothesized and has been evolving into a more clonal species, driven by the use/misuse of antimicrobials. The MDR gonococcal clade should be further investigated for early detection of strains with predispositions to develop and maintain MDR and for initiation of public health interventions.
publishDate 2020
dc.date.none.fl_str_mv 2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://fisabio.portalinvestigacion.com/publicaciones/15231
url https://fisabio.portalinvestigacion.com/publicaciones/15231
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv BMC
publisher.none.fl_str_mv BMC
dc.source.none.fl_str_mv BMC GENOMICS
ISSN: 14712164
reponame:r-FISABIO. Repositorio Institucional de Producción Científica
instname:Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)
instname_str Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)
reponame_str r-FISABIO. Repositorio Institucional de Producción Científica
collection r-FISABIO. Repositorio Institucional de Producción Científica
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869402884050780160
score 15,811543

Similares en LA Referencia