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      Genomic surveillance of Neisseria gonorrhoeae to investigate the distribution and evolution of antimicrobial-resistance determinants and lineages

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          Abstract

          The first extensively drug resistant (XDR) Neisseria gonorrhoeae strain with high resistance to the extended-spectrum cephalosporin ceftriaxone was identified in 2009 in Japan, but no other strain with this antimicrobial-resistance profile has been reported since. However, surveillance to date has been based on phenotypic methods and sequence typing, not genome sequencing. Therefore, little is known about the local population structure at the genomic level, and how resistance determinants and lineages are distributed and evolve. We analysed the whole-genome sequence data and the antimicrobial-susceptibility testing results of 204 strains sampled in a region where the first XDR ceftriaxone-resistant N. gonorrhoeae was isolated, complemented with 67 additional genomes from other time frames and locations within Japan. Strains resistant to ceftriaxone were not found, but we discovered a sequence type (ST)7363 sub-lineage susceptible to ceftriaxone and cefixime in which the mosaic penA allele responsible for reduced susceptibility had reverted to a susceptible allele by recombination. Approximately 85 % of isolates showed resistance to fluoroquinolones (ciprofloxacin) explained by linked amino acid substitutions at positions 91 and 95 of GyrA with 99 % sensitivity and 100 % specificity. Approximately 10 % showed resistance to macrolides (azithromycin), for which genetic determinants are less clear. Furthermore, we revealed different evolutionary paths of the two major lineages: single acquisition of penA X in the ST7363-associated lineage, followed by multiple independent acquisitions of the penA X and XXXIV in the ST1901-associated lineage. Our study provides a detailed picture of the distribution of resistance determinants and disentangles the evolution of the two major lineages spreading worldwide.

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data.

            Open-source bacterial genome assembly remains inaccessible to many biologists because of its complexity. Few software solutions exist that are capable of automating all steps in the process of de novo genome assembly from Illumina data.
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              ClonalFrameML: Efficient Inference of Recombination in Whole Bacterial Genomes

              Recombination is an important evolutionary force in bacteria, but it remains challenging to reconstruct the imports that occurred in the ancestry of a genomic sample. Here we present ClonalFrameML, which uses maximum likelihood inference to simultaneously detect recombination in bacterial genomes and account for it in phylogenetic reconstruction. ClonalFrameML can analyse hundreds of genomes in a matter of hours, and we demonstrate its usefulness on simulated and real datasets. We find evidence for recombination hotspots associated with mobile elements in Clostridium difficile ST6 and a previously undescribed 310kb chromosomal replacement in Staphylococcus aureus ST582. ClonalFrameML is freely available at http://clonalframeml.googlecode.com/.
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                Author and article information

                Journal
                Microb Genom
                Microb Genom
                mgen
                mgen
                Microbial Genomics
                Microbiology Society
                2057-5858
                August 2018
                31 July 2018
                31 July 2018
                : 4
                : 8
                : e000205
                Affiliations
                [ 1]Antimicrobial Resistance Research Center, National Institute of Infectious Diseases , Tokyo, Japan
                [ 2]Department of Bacteriology I, National Institute of Infectious Diseases , Tokyo, Japan
                [ 3]Virology Section, Division of Microbiology, Osaka Institute of Public Health , Osaka, Japan
                [ 4]Department of Microbiology, Kanagawa Prefectural Institute of Public Health , Kanagawa, Japan
                [ 5]Department of Urology, Graduate School of Medicine, Gifu University , Gifu, Japan
                [ 6]Department of Infectious Disease Epidemiology, Imperial College , London, UK
                [ ]Present address: Faculty of Veterinary Medicine, Okayama University of Science, 1-3, Ikoinooka, Imabari, Ehime 794-8555, Japan.
                Author notes
                *Correspondence: Koji Yahara, k-yahara@ 123456nih.go.jp
                Article
                mgen000205
                10.1099/mgen.0.000205
                6159555
                30063202
                90c5223e-5bee-4ef6-91ac-8a09536356e2
                © 2018 The Authors

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 16 May 2018
                : 09 July 2018
                Funding
                Funded by: Ministry of Education, Culture, Sports, Science and Technology
                Award ID: 18K17406
                Funded by: Japan Agency for Medical Research and Development
                Award ID: JP18fk0108062
                Categories
                Research Article
                Microbial Evolution and Epidemiology: Population Genomics
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                antimicrobial resistance,genomic epidemiology,phylogeny,recombination,neisseria gonorrhoeae,surveillance,cephalosporin,macrolide,fluoroquinolone,coalescent

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