{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T21:18:43Z","timestamp":1780521523842,"version":"3.54.1"},"reference-count":40,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2024,10,12]],"date-time":"2024-10-12T00:00:00Z","timestamp":1728691200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Science Center","award":["2017\/27\/B\/NZ7\/00040)"],"award-info":[{"award-number":["2017\/27\/B\/NZ7\/00040)"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,3,17]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>The antibiotic resistance determinants and associated mobile genetic elements (MGEs) were detected among Streptococcus pyogenes (group A streptococci [GAS]) clinical isolates of an M77 serotype collected in Poland between 2003 and 2017.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>The genomes of 136 M77 GAS isolates were sequenced using short- and selected with long-read approach; whole genome sequences were analyzed to determine the genetic context of macrolide resistance determinants.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>The analysed strains were collected from in- and outpatients. Sequencing data analysis revealed that all strains carried the tet(O) gene. They were classified as a single sequence type, ST63. The unique erythromycin-resistance determinant, the erm(TR), was detected in 76.5% (n = 104) of isolates. It was found predominantly (n = 74) within a novel hybrid integrative conjugative element composed of the ICESp1108-like sequence and ICESp2906 variant, which was then named ICESp1109. However, in strains isolated before 2008, erm(TR) was located within ICESp2905 (n = 27) and in 3 strains - within stand-alone ICESp1108-like sequences.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>Based on phylogenetic analysis results, the clonal dissemination of the macrolide-resistant S. pyogenes M77\/ST63 strain with hybrid ICESp1109 was observed between 2008 and 2017. ICESp1109 is the novel hybrid ICE in gram-positive bacteria.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/infdis\/jiae473","type":"journal-article","created":{"date-parts":[[2024,10,12]],"date-time":"2024-10-12T00:01:27Z","timestamp":1728691287000},"page":"e521-e530","source":"Crossref","is-referenced-by-count":3,"title":["ICE<i>Sp1109<\/i>, a Novel Hybrid Integrative Conjugative Element of Macrolide-Resistant <i>Streptococcus pyogenes<\/i> Serotype M77 Collected Between 2003 and 2017 in Poland"],"prefix":"10.1093","volume":"231","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3800-2557","authenticated-orcid":false,"given":"Jan","family":"Gawor","sequence":"first","affiliation":[{"name":"Institute of Biochemistry and Biophysics, Polish Academy of Sciences , Warsaw ,","place":["Poland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7097-4025","authenticated-orcid":false,"given":"Karolina","family":"\u017buchniewicz","sequence":"additional","affiliation":[{"name":"Institute of Biochemistry and Biophysics, Polish Academy of Sciences , Warsaw ,","place":["Poland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2044-4560","authenticated-orcid":false,"given":"Matthew","family":"Ojeda Saavedra","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular and Translational Human Infectious Disease Research, Center for Infectious Diseases, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute and Houston Methodist Hospital , Houston, Texas ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3041-0185","authenticated-orcid":false,"given":"Stephen B","family":"Beres","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular and Translational Human Infectious Disease Research, Center for Infectious Diseases, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute and Houston Methodist Hospital , Houston, Texas ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2318-3375","authenticated-orcid":false,"given":"Marlena","family":"Kiedrowska","sequence":"additional","affiliation":[{"name":"Department of Epidemiology and Clinical Microbiology, National Institute of Medicines"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4726-5984","authenticated-orcid":false,"given":"Izabela","family":"Wr\u00f3bel-Pawelczyk","sequence":"additional","affiliation":[{"name":"Department of Epidemiology and Clinical Microbiology, National Institute of Medicines"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6949-4860","authenticated-orcid":false,"given":"Aleksandra","family":"Kozi\u0144ska","sequence":"additional","affiliation":[{"name":"Department of Epidemiology and Clinical Microbiology, National Institute of Medicines"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9941-6692","authenticated-orcid":false,"given":"Robert","family":"Gromadka","sequence":"additional","affiliation":[{"name":"Institute of Biochemistry and Biophysics, Polish Academy of Sciences , Warsaw ,","place":["Poland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7765-4956","authenticated-orcid":false,"given":"James M","family":"Musser","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular and Translational Human Infectious Disease Research, Center for Infectious Diseases, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute and Houston Methodist Hospital , Houston, Texas ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8228-9917","authenticated-orcid":false,"given":"Izabela","family":"Sitkiewicz","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Microbiology, Warsaw University of Life Sciences , Warsaw ,","place":["Poland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3452-8167","authenticated-orcid":false,"given":"Izabela","family":"Kern-Zdanowicz","sequence":"additional","affiliation":[{"name":"Institute of Biochemistry and Biophysics, Polish Academy of Sciences , Warsaw ,","place":["Poland"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,10,12]]},"reference":[{"key":"2025031709184590500_jiae473-B1","volume-title":"Streptococcus pyogenes: basic biology to clinical manifestations","author":"Craik","year":"2022","edition":"2nd ed"},{"key":"2025031709184590500_jiae473-B2","volume-title":"Streptococcus pyogenes: basic biology to clinical manifestations","author":"Stevens","year":"2022","edition":"2nd ed"},{"key":"2025031709184590500_jiae473-B3","volume-title":"Streptococcus pyogenes: basic biology to clinical manifestations","author":"Cattoir","year":"2022","edition":"2nd ed"},{"key":"2025031709184590500_jiae473-B4","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1021\/acsinfecdis.7b00251","article-title":"Antibiotic resistance ABC-F proteins: bringing target protection into the limelight","volume":"4","author":"Sharkey","year":"2018","journal-title":"ACS Infect Dis"},{"key":"2025031709184590500_jiae473-B5","author":"Wozniak"},{"key":"2025031709184590500_jiae473-B6","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1128\/AAC.05352-11","article-title":"ICESp2905, the erm(TR)-tet(O) element of Streptococcus pyogenes, is formed by two independent integrative and conjugative elements","volume":"56","author":"Giovanetti","year":"2012","journal-title":"Antimicrob Agents Chemother"},{"key":"2025031709184590500_jiae473-B7","doi-asserted-by":"crossref","first-page":"2106","DOI":"10.1128\/AAC.01378-10","article-title":"Two distinct genetic elements are responsible for erm(TR)-mediated erythromycin resistance in tetracycline-susceptible and tetracycline-resistant strains of Streptococcus pyogenes","volume":"55","author":"Brenciani","year":"2011","journal-title":"Antimicrob Agents Chemother"},{"key":"2025031709184590500_jiae473-B8","doi-asserted-by":"crossref","first-page":"e0232777","DOI":"10.1371\/journal.pone.0232777","article-title":"Emm types and clusters and macrolide resistance of pediatric group A streptococcal isolates in central Greece during 2011\u20132017","volume":"15","author":"Grivea","year":"2020","journal-title":"PLoS One."},{"key":"2025031709184590500_jiae473-B9","doi-asserted-by":"crossref","first-page":"1797","DOI":"10.1007\/s10096-015-2414-x","article-title":"Decline in macrolide resistance rates among Streptococcus pyogenes causing pharyngitis in children isolated in Italy","volume":"34","author":"Gherardi","year":"2015","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"2025031709184590500_jiae473-B10","doi-asserted-by":"crossref","first-page":"1991","DOI":"10.1093\/jac\/dkab130","article-title":"Deciphering mobile genetic elements disseminating macrolide resistance in Streptococcus pyogenes over a 21 year period in Barcelona, Spain","volume":"76","author":"Berbel","year":"2021","journal-title":"J Antimicrob Chemother"},{"key":"2025031709184590500_jiae473-B11","doi-asserted-by":"crossref","first-page":"4371","DOI":"10.1073\/pnas.0911295107","article-title":"Molecular complexity of successive bacterial epidemics deconvoluted by comparative pathogenomics","volume":"107","author":"Beres","year":"2010","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2025031709184590500_jiae473-B12","doi-asserted-by":"crossref","first-page":"1474","DOI":"10.1093\/jac\/dku039","article-title":"What causes decreased erythromycin resistance in Streptococcus pyogenes? Dynamics of four clones in a southern European region from 2005 to 2012","volume":"69","author":"Montes","year":"2014","journal-title":"J Antimicrob Chemother"},{"key":"2025031709184590500_jiae473-B13","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1093\/jac\/dkh420","article-title":"A rapid increase in macrolide resistance in Streptococcus pyogenes isolated in Poland during 1996\u20132002","volume":"54","author":"Szczypa","year":"2004","journal-title":"J Antimicrob Chemother"},{"key":"2025031709184590500_jiae473-B14","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1007\/s13353-024-00875-y","article-title":"Epidemiology of Streptococcus pyogenes upper respiratory tract infections in Poland (2003\u20132017)","volume":"65","author":"Sitkiewicz","year":"2024","journal-title":"J Appl Genet"},{"key":"2025031709184590500_jiae473-B15","doi-asserted-by":"crossref","first-page":"2199","DOI":"10.1016\/j.vaccine.2010.09.100","article-title":"The current status of invasive pneumococcal disease in Poland","volume":"29","author":"Skoczy\u0144ska","year":"2011","journal-title":"Vaccine"},{"key":"2025031709184590500_jiae473-B16","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1111\/j.1469-0691.2007.01664.x","article-title":"Resistance patterns of selected respiratory tract pathogens in Poland","volume":"13","author":"Skoczy\u0144ska","year":"2007","journal-title":"Clin Microbiol Infect"},{"issue":"D1","key":"2025031709184590500_jiae473-B17","doi-asserted-by":"crossref","first-page":"D566","DOI":"10.1093\/nar\/gkw1004","article-title":"CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database","volume":"45","author":"Jia","year":"2017","journal-title":"Nucleic Acids Res"},{"issue":"Database issue","key":"2025031709184590500_jiae473-B18","doi-asserted-by":"crossref","first-page":"D325","DOI":"10.1093\/nar\/gki008","article-title":"VFDB: a reference database for bacterial virulence factors","volume":"33","author":"Chen","year":"2005","journal-title":"Nucleic Acids Res"},{"key":"2025031709184590500_jiae473-B19","doi-asserted-by":"crossref","first-page":"e15","DOI":"10.1093\/nar\/gku1196","article-title":"Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins","volume":"43","author":"Croucher","year":"2015","journal-title":"Nucleic Acids Res"},{"key":"2025031709184590500_jiae473-B20","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1093\/jac\/dkaa390","article-title":"Detection of mobile genetic elements associated with antibiotic resistance in Salmonella enterica using a newly developed web tool: MobileElementFinder","volume":"76","author":"Johansson","year":"2021","journal-title":"J Antimicrob Chemother"},{"issue":"D1","key":"2025031709184590500_jiae473-B21","doi-asserted-by":"crossref","first-page":"D660","DOI":"10.1093\/nar\/gky1123","article-title":"ICEberg 2.0: an updated database of bacterial integrative and conjugative elements","volume":"47","author":"Liu","year":"2019","journal-title":"Nucleic Acids Res"},{"issue":"W1","key":"2025031709184590500_jiae473-B22","doi-asserted-by":"crossref","first-page":"W768","DOI":"10.1093\/nar\/gkac321","article-title":"VRprofile2: detection of antibiotic resistance-associated mobilome in bacterial pathogens","volume":"50","author":"Wang","year":"2022","journal-title":"Nucleic Acids Res"},{"key":"2025031709184590500_jiae473-B23","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1186\/1471-2105-10-421","article-title":"BLAST+: architecture and applications","volume":"10","author":"Camacho","year":"2009","journal-title":"BMC Bioinformatics"},{"key":"2025031709184590500_jiae473-B24","doi-asserted-by":"crossref","first-page":"4658","DOI":"10.1073\/pnas.071559398","article-title":"Complete genome sequence of an M1 strain of Streptococcus pyogenes","volume":"98","author":"Ferretti","year":"2001","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2025031709184590500_jiae473-B25","doi-asserted-by":"crossref","first-page":"e02521","DOI":"10.1128\/mBio.02521-19","article-title":"The emergence of successful Streptococcus pyogenes lineages through convergent pathways of capsule loss and recombination directing high toxin expression","volume":"10","author":"Turner","year":"2019","journal-title":"MBio"},{"key":"2025031709184590500_jiae473-B26","doi-asserted-by":"crossref","first-page":"e00638","DOI":"10.1128\/JCM.00638-20","article-title":"Population genomic molecular epidemiological study of macrolide-resistant Streptococcus pyogenes in Iceland, 1995 to 2016: identification of a large clonal population with a pbp2x mutation conferring reduced in vitro \u03b2-lactam susceptibility","volume":"58","author":"Southon","year":"2020","journal-title":"J Clin Microbiol"},{"key":"2025031709184590500_jiae473-B27","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1128\/JCM.39.2.586-590.2001","article-title":"Unusual occurrence of M type 77, antibiotic-resistant group A streptococci in southern Sweden","volume":"39","author":"Jasir","year":"2001","journal-title":"J Clin Microbiol"},{"key":"2025031709184590500_jiae473-B28","doi-asserted-by":"crossref","first-page":"e0361821","DOI":"10.1128\/mbio.03618-21","article-title":"Integrative reverse genetic analysis identifies polymorphisms contributing to decreased antimicrobial agent susceptibility in Streptococcus pyogenes","volume":"13","author":"Beres","year":"2022","journal-title":"MBio"},{"key":"2025031709184590500_jiae473-B29","doi-asserted-by":"crossref","first-page":"1477","DOI":"10.1038\/ncomms2470","article-title":"Mechanism of tetracycline resistance by ribosomal protection protein Tet(O)","volume":"4","author":"Li","year":"2013","journal-title":"Nat Commun"},{"key":"2025031709184590500_jiae473-B30","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1093\/jac\/dkm120","article-title":"New Tn916-related elements causing erm(B)-mediated erythromycin resistance in tetracycline-susceptible pneumococci","volume":"60","author":"Cochetti","year":"2007","journal-title":"J Antimicrob Chemother"},{"key":"2025031709184590500_jiae473-B31","doi-asserted-by":"crossref","first-page":"24123","DOI":"10.1074\/jbc.271.39.24123","article-title":"Energetics and mechanism of drug transport mediated by the lactococcal multidrug transporter LmrP","volume":"271","author":"Bolhuis","year":"1996","journal-title":"J Biol Chem"},{"key":"2025031709184590500_jiae473-B32","doi-asserted-by":"crossref","first-page":"MDNA3-0030-2014","DOI":"10.1128\/microbiolspec.MDNA3-0030-2014","article-title":"Everyman's guide to bacterial insertion sequences","volume":"3","author":"Siguier","year":"2015","journal-title":"Microbiol Spectr"},{"key":"2025031709184590500_jiae473-B33","doi-asserted-by":"crossref","first-page":"1979","DOI":"10.1128\/JB.01745-12","article-title":"Modular evolution of TnGBSs, a new family of integrative and conjugative elements associating insertion sequence transposition, plasmid replication, and conjugation for their spreading","volume":"195","author":"Gu\u00e9rillot","year":"2013","journal-title":"J Bacteriol"},{"key":"2025031709184590500_jiae473-B34","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/j.tim.2009.03.002","article-title":"A modular master on the move: the Tn916 family of mobile genetic elements","volume":"17","author":"Roberts","year":"2009","journal-title":"Trends Microbiol"},{"key":"2025031709184590500_jiae473-B35","doi-asserted-by":"crossref","first-page":"760","DOI":"10.1086\/430618","article-title":"Genome sequence of a serotype M28 strain of group A Streptococcus: potential new insights into puerperal sepsis and bacterial disease specificity","volume":"192","author":"Green","year":"2005","journal-title":"J Infect Dis"},{"key":"2025031709184590500_jiae473-B36","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1186\/1471-2180-11-65","article-title":"Lateral gene transfer of streptococcal ICE element RD2 (region of difference 2) encoding secreted proteins","volume":"11","author":"Sitkiewicz","year":"2011","journal-title":"BMC Microbiol"},{"key":"2025031709184590500_jiae473-B37","doi-asserted-by":"crossref","first-page":"e0072220","DOI":"10.1128\/IAI.00722-20","article-title":"The RD2 pathogenicity island modifies the disease potential of the group A Streptococcus","volume":"89","author":"Roshika","year":"2021","journal-title":"Infect Immun"},{"key":"2025031709184590500_jiae473-B38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fmicb.2015.01483","article-title":"New insights into the classification and integration specificity of Streptococcus integrative conjugative elements through extensive genome exploration","volume":"6","author":"Ambroset","year":"2016","journal-title":"Front Microbiol"},{"key":"2025031709184590500_jiae473-B39","doi-asserted-by":"crossref","first-page":"7059","DOI":"10.1073\/pnas.0510279103","article-title":"Molecular genetic anatomy of inter- and intraserotype variation in the human bacterial pathogen group A Streptococcus","volume":"103","author":"Beres","year":"2006","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2025031709184590500_jiae473-B40","author":"World Health Organization"}],"container-title":["The Journal of Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jid\/advance-article-pdf\/doi\/10.1093\/infdis\/jiae473\/59813869\/jiae473.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jid\/article-pdf\/231\/3\/e521\/59813869\/jiae473.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jid\/article-pdf\/231\/3\/e521\/59813869\/jiae473.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,17]],"date-time":"2025-03-17T09:19:19Z","timestamp":1742203159000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jid\/article\/231\/3\/e521\/7818965"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,12]]},"references-count":40,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2024,10,12]]},"published-print":{"date-parts":[[2025,3,17]]}},"URL":"https:\/\/doi.org\/10.1093\/infdis\/jiae473","relation":{},"ISSN":["0022-1899","1537-6613"],"issn-type":[{"value":"0022-1899","type":"print"},{"value":"1537-6613","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,3,15]]},"published":{"date-parts":[[2024,10,12]]}}}