{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T20:26:41Z","timestamp":1790022401733,"version":"4.0.1"},"reference-count":49,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2025,12,8]],"date-time":"2025-12-08T00:00:00Z","timestamp":1765152000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"state assignment","award":["388-00083-25-03"],"award-info":[{"award-number":["388-00083-25-03"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Background\/Objectives:\u00a0Providencia stuartii is intrinsically resistant to several antibiotic classes, and acquisition of blaNDM further restricts treatment options. This study aimed to characterize NDM-producing P. stuartii isolates from a small hospital cluster in Russia and to place them within the global genomic context. Methods: Four isolates recovered between June and July 2023 from a single hospital were analyzed using Illumina and Oxford Nanopore sequencing to assess genetic relatedness and plasmid content. Results: The isolates showed identical extensively drug-resistant profiles and were closely related genomically. All carried nearly identical IncC plasmids harboring multiple antimicrobial resistance genes, including blaNDM. Comparative analysis indicated that these genomes clustered with recent European isolates but differed in the blaNDM allele and its genomic location. Highly similar IncC plasmids were also found in our previous Klebsiella pneumoniae dataset, demonstrating that this plasmid backbone occurs in multiple bacterial species in the region. Conclusions: The study highlights the role of IncC plasmids in carbapenemase dissemination and underscores the value of genomic surveillance integrating chromosomal and plasmid analyses to track extensively drug-resistant pathogens.<\/jats:p>","DOI":"10.3390\/antibiotics14121238","type":"journal-article","created":{"date-parts":[[2025,12,8]],"date-time":"2025-12-08T14:52:24Z","timestamp":1765205544000},"page":"1238","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Genomic Characterization of NDM-1 Producer Providencia stuartii Isolated in Russia"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6915-031X","authenticated-orcid":false,"given":"Valeria V.","family":"Shapovalova","sequence":"first","affiliation":[{"name":"Federal State Budgetary Institution \u00abCentre for Strategic Planning and Management of Biomedical Health Risks\u00bb of the Federal Medical Biological Agency, 119121 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3963-0144","authenticated-orcid":false,"given":"Vladimir A.","family":"Ageevets","sequence":"additional","affiliation":[{"name":"Federal Research and Clinical Center for Infectious Diseases, 197022 Saint Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3549-3525","authenticated-orcid":false,"given":"Irina V.","family":"Ageevets","sequence":"additional","affiliation":[{"name":"Federal Research and Clinical Center for Infectious Diseases, 197022 Saint Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alisa A.","family":"Avdeeva","sequence":"additional","affiliation":[{"name":"Federal Research and Clinical Center for Infectious Diseases, 197022 Saint Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ofeliia S.","family":"Sulian","sequence":"additional","affiliation":[{"name":"Federal Research and Clinical Center for Infectious Diseases, 197022 Saint Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6301-9169","authenticated-orcid":false,"given":"Alina D.","family":"Matsvay","sequence":"additional","affiliation":[{"name":"Federal State Budgetary Institution \u00abCentre for Strategic Planning and Management of Biomedical Health Risks\u00bb of the Federal Medical Biological Agency, 119121 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuliya A.","family":"Savochkina","sequence":"additional","affiliation":[{"name":"Federal State Budgetary Institution \u00abCentre for Strategic Planning and Management of Biomedical Health Risks\u00bb of the Federal Medical Biological Agency, 119121 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0210-1668","authenticated-orcid":false,"given":"Ekaterina N.","family":"Belyakova","sequence":"additional","affiliation":[{"name":"Federal State Budgetary Institution \u00abCentre for Strategic Planning and Management of Biomedical Health Risks\u00bb of the Federal Medical Biological Agency, 119121 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"German A.","family":"Shipulin","sequence":"additional","affiliation":[{"name":"Federal State Budgetary Institution \u00abCentre for Strategic Planning and Management of Biomedical Health Risks\u00bb of the Federal Medical Biological Agency, 119121 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3550-7875","authenticated-orcid":false,"given":"Sergey V.","family":"Sidorenko","sequence":"additional","affiliation":[{"name":"Federal Research and Clinical Center for Infectious Diseases, 197022 Saint Petersburg, Russia"},{"name":"Department of Medical Microbiology, North-Western State Medical University Named After I.I. Mechnikov, 191015 Saint Petersburg, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,12,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1128\/CMR.13.4.534","article-title":"Classification, Identification, and Clinical Significance of Proteus, Providencia, and Morganella","volume":"13","author":"Brenner","year":"2000","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"810","DOI":"10.1016\/j.tim.2025.02.009","article-title":"Providencia\u00a0stuartii","volume":"33","author":"Witteveen","year":"2025","journal-title":"Trends Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.1038\/s41467-022-28819-2","article-title":"Role of Mobile Genetic Elements in the Global Dissemination of the Carbapenem Resistance Gene blaNDM","volume":"13","author":"Acman","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Alglave, L., Faure, K., and Mulli\u00e9, C. (2025). Plasmid Dissemination in Multispecies Carbapenemase-Producing Enterobacterales Outbreaks Involving Clinical and Environmental Strains: A Narrative Review. Microorganisms, 13.","DOI":"10.3390\/microorganisms13040810"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Fang, L., Chen, R., Li, C., Sun, J., Liu, R., Shen, Y., and Guo, X. (2024). The Association between the Genetic Structures of Commonly Incompatible Plasmids in Gram-Negative Bacteria, Their Distribution and the Resistance Genes. Front. Cell. Infect. Microbiol., 14.","DOI":"10.3389\/fcimb.2024.1472876"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"4555","DOI":"10.1038\/s41467-024-48352-8","article-title":"The Evolution of Antibiotic Resistance Islands Occurs within the Framework of Plasmid Lineages","volume":"15","author":"Wang","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e00731-23","DOI":"10.1128\/msphere.00731-23","article-title":"Genomic Revisitation and Reclassification of the Genus Providencia","volume":"9","author":"Dong","year":"2024","journal-title":"mSphere"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e01406-22","DOI":"10.1128\/aac.01406-22","article-title":"Epidemiology of Resistance Determinants Identified in Meropenem-Nonsusceptible Enterobacterales Collected as Part of a Global Surveillance Study, 2018 to 2019","volume":"67","author":"Estabrook","year":"2023","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Guidone, G.H.M., Cardozo, J.G., Silva, L.C., Sanches, M.S., Galhardi, L.C.F., Kobayashi, R.K.T., Vespero, E.C., and Rocha, S.P.D. (2023). Epidemiology and Characterization of Providencia stuartii Isolated from Hospitalized Patients in Southern Brazil: A Possible Emerging Pathogen. Access Microbiol., 5.","DOI":"10.1099\/acmi.0.000652.v4"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.jgar.2023.06.002","article-title":"Genotypic Characterisation of Carbapenemase-Producing Organisms Obtained in Denmark from Patients Associated with the War in Ukraine","volume":"34","author":"Stolberg","year":"2023","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2200896","DOI":"10.2807\/1560-7917.ES.2022.27.50.2200896","article-title":"Multidrug-Resistant Organisms in Patients from Ukraine in the Netherlands, March to August 2022","volume":"27","author":"Zwittink","year":"2022","journal-title":"Eurosurveillance"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1093\/jac\/dkad400","article-title":"Characterization of VIM-29 and VIM-86, Two VIM-1 Variants Isolated in Multidrug-Resistant Enterobacterales in France","volume":"79","author":"Rezzoug","year":"2024","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Capitani, V., Arcari, G., Oliva, A., Sacco, F., Menichincheri, G., Fenske, L., Polani, R., Raponi, G., Antonelli, G., and Carattoli, A. (2023). Genome-Based Retrospective Analysis of a Providencia stuartii Outbreak in Rome, Italy: Broad Spectrum IncC Plasmids Spread the NDM Carbapenemase within the Hospital. Antibiotics, 12.","DOI":"10.3390\/antibiotics12050943"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Sabtcheva, S., Stoikov, I., Ivanov, I.N., Donchev, D., Lesseva, M., Georgieva, S., Teneva, D., Dobreva, E., and Christova, I. (2024). Genomic Characterization of Carbapenemase-Producing Enterobacter hormaechei, Serratia marcescens, Citrobacter freundii, Providencia stuartii, and Morganella morganii Clinical Isolates from Bulgaria. Antibiotics, 13.","DOI":"10.20944\/preprints202404.1794.v1"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2400587","DOI":"10.2807\/1560-7917.ES.2024.29.47.2400587","article-title":"Genomic Surveillance Detects Interregional Spread of New Delhi Metallo-Beta-Lactamase-1-Producing Providencia stuartii in Hospitals, Romania, December 2021 to September 2023","volume":"29","author":"Linkevicius","year":"2024","journal-title":"Eurosurveillance"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2300616","DOI":"10.2807\/1560-7917.ES.2024.29.23.2300616","article-title":"Dissemination of Extensively Drug-Resistant NDM-Producing Providencia stuartii in Europe Linked to Patients Transferred from Ukraine, March 2022 to March 2023","volume":"29","author":"Witteveen","year":"2024","journal-title":"Eurosurveillance"},{"key":"ref_17","unstructured":"European Centre for Disease Prevention and Control (2024). Rapid Investigation of New Delhi Metallo-Beta-Lactamase (NDM)-1-Producing Providencia stuartii in Hospitals in Romania: November 2024, Publications Office."},{"key":"ref_18","unstructured":"WHO Regional Office for Europe, and European Centre for Disease Prevention and Control (2025). Surveillance of Antimicrobial Resistance in Europe, 2024 Data: Executive Summary, WHO Regional Office for Europe."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1769","DOI":"10.1111\/j.1365-2958.2007.05624.x","article-title":"TraA, TraC and TraD Autorepress Two Divergent Quorum-regulated Promoters near the Transfer Origin of the Ti Plasmid of Agrobacterium tumefaciens","volume":"63","author":"Cho","year":"2007","journal-title":"Mol. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"4764","DOI":"10.1038\/s41467-023-39915-2","article-title":"Genomic Dissection of Endemic Carbapenem Resistance Reveals Metallo-Beta-Lactamase Dissemination through Clonal, Plasmid and Integron Transfer","volume":"14","author":"Macesic","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Shapovalova, V.V., Chulkova, P.S., Ageevets, V.A., Nurmukanova, V., Verentsova, I.V., Girina, A.A., Protasova, I.N., Bezbido, V.S., Sergevnin, V.I., and Feldblum, I.V. (2024). High-Risk Lineages of Hybrid Plasmids Carrying Virulence and Carbapenemase Genes. Antibiotics, 13.","DOI":"10.3390\/antibiotics13121224"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Van Der Zee, A., Roorda, L., Bosman, G., Fluit, A.C., Hermans, M., Smits, P.H., Van Der Zanden, A.G., Te Witt, R., Bruijnesteijn Van Coppenraet, L.E., and Cohen Stuart, J. (2014). Multi-Centre Evaluation of Real-Time Multiplex PCR for Detection of Carbapenemase Genes OXA-48, VIM, IMP, NDM and KPC. BMC Infect. Dis., 14.","DOI":"10.1186\/1471-2334-14-27"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Shapovalova, V., Shaidullina, E., Azizov, I., Sheck, E., Martinovich, A., Dyachkova, M., Matsvay, A., Savochkina, Y., Khafizov, K., and Kozlov, R. (2022). Molecular Epidemiology of Mcr-1-Positive Escherichia coli and Klebsiella pneumoniae Isolates: Results from Russian Sentinel Surveillance (2013\u20132018). Microorganisms, 10.","DOI":"10.3390\/microorganisms10102034"},{"key":"ref_24","unstructured":"(2025, December 04). Dorado. Available online: https:\/\/github.com\/nanoporetech\/dorado."},{"key":"ref_25","unstructured":"(2024, November 03). Babraham Bioinformatics\u2014FastQC A Quality Control Tool for High Throughput Sequence Data. Available online: http:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1093\/bioinformatics\/bty654","article-title":"MinIONQC: Fast and Simple Quality Control for MinION Sequencing Data","volume":"35","author":"Lanfear","year":"2019","journal-title":"Bioinformatics"},{"key":"ref_27","unstructured":"Petit, R.A. (2025, December 04). Dragonflye: Assemble Bacterial Isolate Genomes from Nanopore Reads. Available online: https:\/\/github.com\/rpetit3\/dragonflye\/."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1072","DOI":"10.1093\/bioinformatics\/btt086","article-title":"QUAST: Quality Assessment Tool for Genome Assemblies","volume":"29","author":"Gurevich","year":"2013","journal-title":"Bioinformatics"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1043","DOI":"10.1101\/gr.186072.114","article-title":"CheckM: Assessing the Quality of Microbial Genomes Recovered from Isolates, Single Cells, and Metagenomes","volume":"25","author":"Parks","year":"2015","journal-title":"Genome Res."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Wood, D.E., Lu, J., and Langmead, B. (2019). Improved Metagenomic Analysis with Kraken 2. Genome Biol., 20.","DOI":"10.1186\/s13059-019-1891-0"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"D801","DOI":"10.1093\/nar\/gkab902","article-title":"TYGS and LPSN: A Database Tandem for Fast and Reliable Genome-Based Classification and Nomenclature of Prokaryotes","volume":"50","author":"Carbasse","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: Rapid Prokaryotic Genome Annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Feldgarden, M., Brover, V., Gonzalez-Escalona, N., Frye, J.G., Haendiges, J., Haft, D.H., Hoffmann, M., Pettengill, J.B., Prasad, A.B., and Tillman, G.E. (2021). AMRFinderPlus and the Reference Gene Catalog Facilitate Examination of the Genomic Links among Antimicrobial Resistance, Stress Response, and Virulence. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-91456-0"},{"key":"ref_34","first-page":"e000206","article-title":"MOB-Suite: Software Tools for Clustering, Reconstruction and Typing of Plasmids from Draft Assemblies","volume":"4","author":"Robertson","year":"2018","journal-title":"Microb. Genom."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"W229","DOI":"10.1093\/nar\/gky352","article-title":"oriTfinder: A Web-Based Tool for the Identification of Origin of Transfers in DNA Sequences of Bacterial Mobile Genetic Elements","volume":"46","author":"Li","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Treangen, T.J., Ondov, B.D., Koren, S., and Phillippy, A.M. (2014). The Harvest Suite for Rapid Core-Genome Alignment and Visualization of Thousands of Intraspecific Microbial Genomes. Genome Biol., 15.","DOI":"10.1186\/s13059-014-0524-x"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Price, M.N., Dehal, P.S., and Arkin, A.P. (2010). FastTree 2\u2014Approximately Maximum-Likelihood Trees for Large Alignments. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009490"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5539","DOI":"10.1093\/nar\/gkz361","article-title":"Fast Hierarchical Bayesian Analysis of Population Structure","volume":"47","author":"Lees","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Tonkin-Hill, G., MacAlasdair, N., Ruis, C., Weimann, A., Horesh, G., Lees, J.A., Gladstone, R.A., Lo, S., Beaudoin, C., and Floto, R.A. (2020). Producing Polished Prokaryotic Pangenomes with the Panaroo Pipeline. Genome Biol., 21.","DOI":"10.1186\/s13059-020-02090-4"},{"key":"ref_40","first-page":"e000056","article-title":"SNP-Sites: Rapid Efficient Extraction of SNPs from Multi-FASTA Alignments","volume":"2","author":"Page","year":"2016","journal-title":"Microb. Genom."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1093\/molbev\/msaa015","article-title":"IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era","volume":"37","author":"Minh","year":"2020","journal-title":"Mol. Biol. Evol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1038\/nmeth.4285","article-title":"ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates","volume":"14","author":"Kalyaanamoorthy","year":"2017","journal-title":"Nat. Methods"},{"key":"ref_43","first-page":"e000093","article-title":"Microreact: Visualizing and Sharing Data for Genomic Epidemiology and Phylogeography","volume":"2","author":"Abudahab","year":"2016","journal-title":"Microb. Genom."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"W293","DOI":"10.1093\/nar\/gkab301","article-title":"Interactive Tree Of Life (iTOL) v5: An Online Tool for Phylogenetic Tree Display and Annotation","volume":"49","author":"Letunic","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"5114","DOI":"10.1038\/s41467-018-07641-9","article-title":"High Throughput ANI Analysis of 90K Prokaryotic Genomes Reveals Clear Species Boundaries","volume":"9","author":"Jain","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"8005","DOI":"10.1093\/nar\/gkad498","article-title":"Global Transmission of Broad-Host-Range Plasmids Derived from the Human Gut Microbiome","volume":"51","author":"Yang","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e02306-22","DOI":"10.1128\/spectrum.02306-22","article-title":"One Health Analysis of Mcr -Carrying Plasmids and Emergence of Mcr-10.1 in Three Species of Klebsiella Recovered from Humans in China","volume":"10","author":"Liu","year":"2022","journal-title":"Microbiol. Spectr."},{"key":"ref_48","first-page":"001300","article-title":"Applying Rearrangement Distances to Enable Plasmid Epidemiology with Pling","volume":"10","author":"Frolova","year":"2024","journal-title":"Microb. Genom."},{"key":"ref_49","first-page":"e000435","article-title":"Universal Whole-Sequence-Based Plasmid Typing and Its Utility to Prediction of Host Range and Epidemiological Surveillance","volume":"6","author":"Robertson","year":"2020","journal-title":"Microb. Genom."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/14\/12\/1238\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,8]],"date-time":"2025-12-08T15:14:52Z","timestamp":1765206892000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/14\/12\/1238"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,12,8]]},"references-count":49,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["antibiotics14121238"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics14121238","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,12,8]]}}}