{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:07:26Z","timestamp":1760144846653,"version":"build-2065373602"},"reference-count":37,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2024,5,26]],"date-time":"2024-05-26T00:00:00Z","timestamp":1716681600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["24-25-20084"],"award-info":[{"award-number":["24-25-20084"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The increasing problem of antimicrobial resistance in N. gonorrhoeae necessitates the development of molecular typing schemes that are suitable for rapid and mass screening. The objective of this study was to design and validate a mini-MLST scheme for N. gonorrhoeae based on global pathogen population data. Using sequences of seven housekeeping genes of 21,402 isolates with known MLSTs from the PubMLST database, we identified eighteen informative polymorphisms and obtained mini-MLST nucleotide profiles to predict MLSTs of isolates. We proposed a new MLST grouping system for N. gonorrhoeae based on mini-MLST profiles. Phylogenetic analysis revealed that MLST genogroups are a stable characteristic of the N. gonorrhoeae global population. The proposed grouping system has been shown to bring together isolates with similar antimicrobial susceptibility, as demonstrated by the characteristics of major genogroups. Established MLST prediction algorithms based on nucleotide profiles are now publicly available. The mini-MLST scheme was evaluated using a MLST detection\/prediction method based on the original hydrogel DNA microarray. The results confirmed a high predictive ability up to the MLST genogroup. The proposed holistic approach to gonococcal population analysis can be used for the continuous surveillance of known and emerging resistant N. gonorrhoeae isolates.<\/jats:p>","DOI":"10.3390\/ijms25115781","type":"journal-article","created":{"date-parts":[[2024,5,27]],"date-time":"2024-05-27T10:14:07Z","timestamp":1716804847000},"page":"5781","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Mini-Multilocus Sequence Typing Scheme for the Global Population of Neisseria gonorrhoeae"],"prefix":"10.3390","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9416-875X","authenticated-orcid":false,"given":"Ilya","family":"Kandinov","sequence":"first","affiliation":[{"name":"Center for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0316-2262","authenticated-orcid":false,"given":"Boris","family":"Shaskolskiy","sequence":"additional","affiliation":[{"name":"Center for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dmitry","family":"Kravtsov","sequence":"additional","affiliation":[{"name":"Center for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marina","family":"Filippova","sequence":"additional","affiliation":[{"name":"Center for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anatoliy","family":"Larkin","sequence":"additional","affiliation":[{"name":"Center for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3183-318X","authenticated-orcid":false,"given":"Dmitry","family":"Gryadunov","sequence":"additional","affiliation":[{"name":"Center for Precision Genome Editing and Genetic Technologies for Biomedicine, Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,5,26]]},"reference":[{"key":"ref_1","unstructured":"World Health Organization (2024, February 09). Enhanced Gonococcal Antimicrobial Surveillance Programme (EGASP): Surveillance Report 2022. Available online: https:\/\/www.who.int\/publications\/i\/item\/9789240088528."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Jacobsson, S., Cole, M.J., Spiteri, G., Day, M., Unemo, M., and Euro-GASP Network (2021). Associations between antimicrobial susceptibility\/resistance of Neisseria gonorrhoeae isolates in European Union\/European Economic Area and patients\u2019 gender, sexual orientation and anatomical site of infection, 2009\u20132016. BMC Infect. Dis., 21.","DOI":"10.1186\/s12879-021-05931-0"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1080\/22221751.2021.2011618","article-title":"Dissemination and genome analysis of high-level ceftriaxone-resistant penA 60.001 Neisseria gonorrhoeae strains from the Guangdong Gonococcal antibiotics susceptibility Programme (GD-GASP), 2016\u20132019","volume":"11","author":"Lin","year":"2022","journal-title":"Emerg. Microbes Infect."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1080\/14737159.2022.2015329","article-title":"Antimicrobial resistance prediction in Neisseria gonorrhoeae: Current status and future prospects","volume":"22","author":"Golparian","year":"2022","journal-title":"Expert Rev. Mol. Diagn."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1016\/S2666-5247(22)00044-1","article-title":"Europe-wide expansion and eradication of multidrug-resistant Neisseria gonorrhoeae lineages: A genomic surveillance study","volume":"3","author":"Cole","year":"2022","journal-title":"Lancet Microbe"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Kandinov, I., Dementieva, E., Filippova, M., Vinokurova, A., Gorshkova, S., Kubanov, A., Solomka, V., Shagabieva, J., Deryabin, D., and Shaskolskiy, B. (2023). Emergence of Azithromycin-Resistant Neisseria gonorrhoeae Isolates Belonging to the NG-MAST Genogroup 12302 in Russia. Microorganisms, 11.","DOI":"10.3390\/microorganisms11051226"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1071\/SH22118","article-title":"The changing epidemiology of Neisseria gonorrhoeae genogroups and antimicrobial resistance in Queensland, Australia, 2010\u201315: A case series analysis of unique Neisseria gonorrhoeae isolates","volume":"20","author":"Mchugh","year":"2023","journal-title":"Sex. Health"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1128\/CMR.00040-10","article-title":"Review and international recommendation of methods for typing neisseria gonorrhoeae isolates and their implications for improved knowledge of gonococcal epidemiology, treatment, and biology","volume":"24","author":"Unemo","year":"2011","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/j.jinf.2018.02.011","article-title":"Neisseria gonorrhoeae molecular typing for understanding sexual networks and antimicrobial resistance transmission: A systematic review","volume":"76","author":"Town","year":"2018","journal-title":"J. Infect."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1038\/nrmicro3093","article-title":"MLST revisited: The gene-by-gene approach to bacterial genomics","volume":"11","author":"Maiden","year":"2013","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3140","DOI":"10.1073\/pnas.95.6.3140","article-title":"Multilocus sequence typing: A portable approach to the identification of clones within populations of pathogenic\u2009microorganisms","volume":"95","author":"Maiden","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"124","DOI":"10.12688\/wellcomeopenres.14826.1","article-title":"Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications","volume":"3","author":"Jolley","year":"2018","journal-title":"Wellcome Open Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e478","DOI":"10.1016\/S2666-5247(23)00370-1","article-title":"Antimicrobial-resistant Neisseria gonorrhoeae in Europe in 2020 compared with in 2013 and 2018: A retrospective genomic surveillance study","volume":"5","author":"Golparian","year":"2024","journal-title":"Lancet Microbe"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1186\/s13073-021-00860-8","article-title":"Emergence and evolution of antimicrobial resistance genes and mutations in Neisseria gonorrhoeae","volume":"13","author":"Yahara","year":"2021","journal-title":"Genome Med."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.1099\/jmm.0.074286-0","article-title":"A Neisseria gonorrhoeae strain with a meningococcal mtrR sequence","volume":"63","author":"Trembizki","year":"2014","journal-title":"J. Med. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Joseph, S.J., Thomas, J.C., Schmerer, M.W., Cartee, J.C., St. Cyr, S., Schlanger, K., Kersh, E.N., Raphael, B.H., Gernert, K.M., and Antimicrobial Resistant Neisseria Gonorrhoeae Working Group (2022). Global Emergence and Dissemination of Neisseria gonorrhoeae ST-9363 Isolates with Reduced Susceptibility to Azithromycin. Genome Biol. Evol., 14.","DOI":"10.1093\/gbe\/evab287"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3744","DOI":"10.1128\/AAC.46.12.3744-3749.2002","article-title":"Mosaic-Like Structure of Penicillin-Binding Protein 2 Gene (penA) in Clinical Isolates of Neisseria gonorrhoeae with Reduced Susceptibility to Cefixime","volume":"46","author":"Ameyama","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"804","DOI":"10.3201\/eid2404.171817","article-title":"Cephalosporin-Resistant Neisseria gonorrhoeae Clone, China","volume":"24","author":"Chen","year":"2018","journal-title":"Emerg. Infect. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"107101","DOI":"10.1016\/j.ijantimicag.2024.107101","article-title":"penA profile of Neisseria gonorrhoeae in Guangdong, China: Novel penA alleles are related to decreased susceptibility to ceftriaxone or cefixime","volume":"63","author":"Liao","year":"2024","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Wang, D., Wang, Y., Li, Y., Xiu, L., Yong, G., Yang, Y., Gu, W., and Peng, J. (2023). Identification of ceftriaxone-resistant Neisseria gonorrhoeae FC428 clone and isolates harboring a novel mosaic penA gene in Chengdu in 2019\u20132020. Ann. Clin. Microbiol. Antimicrob., 22.","DOI":"10.1186\/s12941-023-00614-x"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"623","DOI":"10.2217\/fmb.14.24","article-title":"Using multilocus sequence typing to study bacterial variation: Prospects in the genomic era","volume":"9","author":"Jolley","year":"2014","journal-title":"Future Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1016\/j.jinf.2016.08.010","article-title":"Genomic analyses of Neisseria gonorrhoeae reveal an association of the gonococcal genetic island with antimicrobial resistance","volume":"73","author":"Harrison","year":"2016","journal-title":"J. Infect."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Nykrynova, M., Barton, V., Bezdicek, M., Lengerova, M., and Skutkova, H. (2022). Identification of highly variable sequence fragments in unmapped reads for rapid bacterial genotyping. BMC Genom., 23.","DOI":"10.1186\/s12864-022-08550-4"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Dufkova, K., Bezdicek, M., Cuprova, K., Pantuckova, D., Nykrynova, M., Brhelova, E., Kocmanova, I., Hodova, S., Hanslianova, M., and Juren, T. (2022). Sequencing Independent Molecular Typing of Staphylococcus aureus Isolates: Approach for Infection Control and Clonal Characterization. Microbiol. Spectr., 10.","DOI":"10.1128\/spectrum.01817-21"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"16572","DOI":"10.1038\/s41598-021-96148-3","article-title":"Rapid high-resolution melting genotyping scheme for Escherichia coli based on MLST derived single nucleotide polymorphisms","volume":"11","author":"Bezdicek","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1093\/jac\/dks381","article-title":"Real-time PCR genotyping of Neisseria gonorrhoeae isolates using 14 informative single nucleotide polymorphisms on gonococcal housekeeping genes","volume":"68","author":"Whiley","year":"2013","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1526","DOI":"10.1093\/jac\/dkt544","article-title":"High-throughput informative single nucleotide polymorphism-based typing of Neisseria gonorrhoeae using the Sequenom MassARRAY iPLEX platform","volume":"69","author":"Trembizki","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4271","DOI":"10.2147\/IDR.S336212","article-title":"Emergence and Characterization of a Ceftriaxone-Resistant Neisseria gonorrhoeae FC428 Clone Evolving Moderate-Level Resistance to Azithromycin in Shenzhen, China","volume":"14","author":"Zhang","year":"2021","journal-title":"Infect. Drug Resist."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3801","DOI":"10.1038\/s41467-021-24072-1","article-title":"Phylogenomic analysis reveals persistence of gonococcal strains with reduced-susceptibility to extended-spectrum cephalosporins and mosaic penA-34","volume":"12","author":"Thomas","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"179","DOI":"10.3103\/S0891416822040036","article-title":"Diversity of NG-MAST and MLST sequence types in Russian clinical isolates of Neisseria gonorrhoeae carrying the \u00abmosaic\u00bb allele of the penA gene","volume":"37","author":"Kubanov","year":"2022","journal-title":"Mol. Genet. Microbiol. Virol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Dufkova, K., Bezdicek, M., Nykrynova, M., Kocmanova, I., Kubackova, P., Hanslikova, J., Fejkova, K., Mayer, J., and Lengerova, M. (2023). Rapid Identification of Pseudomonas aeruginosa International High-Risk Clones Based on High-Resolution Melting Analysis. Microbiol. Spectr., 11.","DOI":"10.1128\/spectrum.03571-22"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Andersson, P., Tong, S.Y., Bell, J.M., Turnidge, J.D., and Giffard, P.M. (2012). Minim typing-a rapid and low cost MLST based typing tool for Klebsiella pneumoniae. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0033530"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1694","DOI":"10.3201\/eid2808.220071","article-title":"Association of Phylogenomic Relatedness among Neisseria gonorrhoeae Strains with Antimicrobial Resistance, Austria, 2016\u20132020","volume":"28","author":"Schaeffer","year":"2022","journal-title":"Emerg. Infect. Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"4","DOI":"10.32607\/2075-8251-2018-10-2-48-5710.32607\/20758251-2018-10-4-4-18","article-title":"The EIMB Hydrogel Microarray Technology: Thirty Years Later","volume":"10","author":"Gryadunov","year":"2018","journal-title":"Acta Naturae"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1166","DOI":"10.1093\/bioinformatics\/bts091","article-title":"Unipro UGENE: A unified bioinformatics toolkit","volume":"28","author":"Okonechnikov","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Shaskolskiy, B., Kandinov, I., Kravtsov, D., Vinokurova, A., Gorshkova, S., Filippova, M., Kubanov, A., Solomka, V., Deryabin, D., and Dementieva, E. (2021). Hydrogel Droplet Microarray for Genotyping Antimicrobial Resistance Determinants in Neisseria gonorrhoeae Isolates. Polymers, 13.","DOI":"10.3390\/polym13223889"},{"key":"ref_37","unstructured":"Bock, G., and Goode, J. (1998). The Limits of Reductionism in Biology, John Wiley and Sons. Novartis Foundation Symposium."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/11\/5781\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:48:58Z","timestamp":1760107738000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/11\/5781"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,26]]},"references-count":37,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2024,6]]}},"alternative-id":["ijms25115781"],"URL":"https:\/\/doi.org\/10.3390\/ijms25115781","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2024,5,26]]}}}