Genomic Analysis Reveals New Integrative Conjugal Elements and Transposons in GBS Conferring Antimicrobial Resistance
<i>Streptococcus agalactiae</i> or group B streptococcus (GBS) is a leading cause of neonatal sepsis and increasingly found as an invasive pathogen in older patient populations. Beta-lactam antibiotics remain the most effective therapeutic with resistance rarely reported, while the major...
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MDPI AG
2023-03-01
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| Series: | Antibiotics |
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| Online Access: | https://www.mdpi.com/2079-6382/12/3/544 |
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| author | Uzma Basit Khan Edward A. R. Portal Kirsty Sands Stephanie Lo Victoria J. Chalker Elita Jauneikaite Owen B. Spiller |
| author_facet | Uzma Basit Khan Edward A. R. Portal Kirsty Sands Stephanie Lo Victoria J. Chalker Elita Jauneikaite Owen B. Spiller |
| author_sort | Uzma Basit Khan |
| collection | DOAJ |
| description | <i>Streptococcus agalactiae</i> or group B streptococcus (GBS) is a leading cause of neonatal sepsis and increasingly found as an invasive pathogen in older patient populations. Beta-lactam antibiotics remain the most effective therapeutic with resistance rarely reported, while the majority of GBS isolates carry the tetracycline resistance gene <i>tet(M)</i> in fixed genomic positions amongst five predominant clonal clades. In the UK, GBS resistance to clindamycin and erythromycin has increased from 3% in 1991 to 11.9% (clindamycin) and 20.2% (erythromycin), as reported in this study. Here, a systematic investigation of antimicrobial resistance genomic content sought to fully characterise the associated mobile genetic elements within phenotypically resistant GBS isolates from 193 invasive and non-invasive infections of UK adult patients collected during 2014 and 2015. Resistance to erythromycin and clindamycin was mediated by <i>erm(A)</i> (16/193, 8.2%), <i>erm(B)</i> (16/193, 8.2%), <i>mef(A)</i>/<i>msr(D)</i> (10/193, 5.1%), <i>lsa(C)</i> (3/193, 1.5%), <i>lnu(C)</i> (1/193, 0.5%), and <i>erm(T)</i> (1/193, 0.5%) genes. The integrative conjugative elements (ICEs) carrying these genes were occasionally found in combination with high gentamicin resistance mediating genes <i>aac</i>(6′)<i>-aph</i>(2″), aminoglycoside resistance genes (<i>ant</i>(6-Ia), <i>aph</i>(3′-III), and/or <i>aad(E)</i>), alternative tetracycline resistance genes (<i>tet(O)</i> and <i>tet(S)</i>), and/or chloramphenicol resistance gene <i>cat(Q)</i>, mediating resistance to multiple classes of antibiotics. This study provides evidence of the retention of previously reported ICESag37 (<i>n</i> = 4), ICESag236 (<i>n</i> = 2), and ICESpy009 (<i>n</i> = 3), as well as the definition of sixteen novel ICEs and three novel transposons within the GBS lineage, with no evidence of horizontal transfer. |
| first_indexed | 2024-03-11T07:02:03Z |
| format | Article |
| id | doaj.art-ead35406910c4b0180f707e319b5c4ef |
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| issn | 2079-6382 |
| language | English |
| last_indexed | 2024-03-11T07:02:03Z |
| publishDate | 2023-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Antibiotics |
| spelling | doaj.art-ead35406910c4b0180f707e319b5c4ef2023-11-17T09:14:31ZengMDPI AGAntibiotics2079-63822023-03-0112354410.3390/antibiotics12030544Genomic Analysis Reveals New Integrative Conjugal Elements and Transposons in GBS Conferring Antimicrobial ResistanceUzma Basit Khan0Edward A. R. Portal1Kirsty Sands2Stephanie Lo3Victoria J. Chalker4Elita Jauneikaite5Owen B. Spiller6Department of Medical Microbiology, Division of Infection and Immunity, Cardiff University, 6th Floor University Hospital of Wales, Cardiff CF14 4XN, UKDepartment of Medical Microbiology, Division of Infection and Immunity, Cardiff University, 6th Floor University Hospital of Wales, Cardiff CF14 4XN, UKDepartment of Medical Microbiology, Division of Infection and Immunity, Cardiff University, 6th Floor University Hospital of Wales, Cardiff CF14 4XN, UKParasites and Microbes Programme, The Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UKBacterial Reference Department, UK Health Security Agency, London NW9 5DF, UKNIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Department of Infectious Disease, Imperial College London, London W12 0NN, UKDepartment of Medical Microbiology, Division of Infection and Immunity, Cardiff University, 6th Floor University Hospital of Wales, Cardiff CF14 4XN, UK<i>Streptococcus agalactiae</i> or group B streptococcus (GBS) is a leading cause of neonatal sepsis and increasingly found as an invasive pathogen in older patient populations. Beta-lactam antibiotics remain the most effective therapeutic with resistance rarely reported, while the majority of GBS isolates carry the tetracycline resistance gene <i>tet(M)</i> in fixed genomic positions amongst five predominant clonal clades. In the UK, GBS resistance to clindamycin and erythromycin has increased from 3% in 1991 to 11.9% (clindamycin) and 20.2% (erythromycin), as reported in this study. Here, a systematic investigation of antimicrobial resistance genomic content sought to fully characterise the associated mobile genetic elements within phenotypically resistant GBS isolates from 193 invasive and non-invasive infections of UK adult patients collected during 2014 and 2015. Resistance to erythromycin and clindamycin was mediated by <i>erm(A)</i> (16/193, 8.2%), <i>erm(B)</i> (16/193, 8.2%), <i>mef(A)</i>/<i>msr(D)</i> (10/193, 5.1%), <i>lsa(C)</i> (3/193, 1.5%), <i>lnu(C)</i> (1/193, 0.5%), and <i>erm(T)</i> (1/193, 0.5%) genes. The integrative conjugative elements (ICEs) carrying these genes were occasionally found in combination with high gentamicin resistance mediating genes <i>aac</i>(6′)<i>-aph</i>(2″), aminoglycoside resistance genes (<i>ant</i>(6-Ia), <i>aph</i>(3′-III), and/or <i>aad(E)</i>), alternative tetracycline resistance genes (<i>tet(O)</i> and <i>tet(S)</i>), and/or chloramphenicol resistance gene <i>cat(Q)</i>, mediating resistance to multiple classes of antibiotics. This study provides evidence of the retention of previously reported ICESag37 (<i>n</i> = 4), ICESag236 (<i>n</i> = 2), and ICESpy009 (<i>n</i> = 3), as well as the definition of sixteen novel ICEs and three novel transposons within the GBS lineage, with no evidence of horizontal transfer.https://www.mdpi.com/2079-6382/12/3/544group B streptococcusmobile genetic elementsintegrative conjugative element (ICE)macrolide resistanceclonal complex (CC) |
| spellingShingle | Uzma Basit Khan Edward A. R. Portal Kirsty Sands Stephanie Lo Victoria J. Chalker Elita Jauneikaite Owen B. Spiller Genomic Analysis Reveals New Integrative Conjugal Elements and Transposons in GBS Conferring Antimicrobial Resistance Antibiotics group B streptococcus mobile genetic elements integrative conjugative element (ICE) macrolide resistance clonal complex (CC) |
| title | Genomic Analysis Reveals New Integrative Conjugal Elements and Transposons in GBS Conferring Antimicrobial Resistance |
| title_full | Genomic Analysis Reveals New Integrative Conjugal Elements and Transposons in GBS Conferring Antimicrobial Resistance |
| title_fullStr | Genomic Analysis Reveals New Integrative Conjugal Elements and Transposons in GBS Conferring Antimicrobial Resistance |
| title_full_unstemmed | Genomic Analysis Reveals New Integrative Conjugal Elements and Transposons in GBS Conferring Antimicrobial Resistance |
| title_short | Genomic Analysis Reveals New Integrative Conjugal Elements and Transposons in GBS Conferring Antimicrobial Resistance |
| title_sort | genomic analysis reveals new integrative conjugal elements and transposons in gbs conferring antimicrobial resistance |
| topic | group B streptococcus mobile genetic elements integrative conjugative element (ICE) macrolide resistance clonal complex (CC) |
| url | https://www.mdpi.com/2079-6382/12/3/544 |
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