Molecular Characterization of Chimeric <i>Staphylococcus aureus</i> Strains from Waterfowl
<i>Staphylococcus aureus</i> is a versatile pathogen that does not only occur in humans but also in various wild and domestic animals, including several avian species. When characterizing <i>S. aureus</i> isolates from waterfowl, isolates were identified as atypical CC133 by...
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MDPI AG
2024-01-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/12/1/96 |
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| author | Stefan Monecke Sascha D. Braun Maximillian Collatz Celia Diezel Elke Müller Martin Reinicke Adriana Cabal Rosel Andrea T. Feßler Dennis Hanke Igor Loncaric Stefan Schwarz Sonia Cortez de Jäckel Werner Ruppitsch Dolores Gavier-Widén Helmut Hotzel Ralf Ehricht |
| author_facet | Stefan Monecke Sascha D. Braun Maximillian Collatz Celia Diezel Elke Müller Martin Reinicke Adriana Cabal Rosel Andrea T. Feßler Dennis Hanke Igor Loncaric Stefan Schwarz Sonia Cortez de Jäckel Werner Ruppitsch Dolores Gavier-Widén Helmut Hotzel Ralf Ehricht |
| author_sort | Stefan Monecke |
| collection | DOAJ |
| description | <i>Staphylococcus aureus</i> is a versatile pathogen that does not only occur in humans but also in various wild and domestic animals, including several avian species. When characterizing <i>S. aureus</i> isolates from waterfowl, isolates were identified as atypical CC133 by DNA microarray analysis. They differed from previously sequenced CC133 strains in the presence of the collagen adhesin gene <i>cna</i>; some also showed a different capsule type and a deviant <i>spa</i> type. Thus, they were subjected to whole-genome sequencing. This revealed multiple insertions of large regions of DNA from other <i>S. aureus</i> lineages into a CC133-derived backbone genome. Three distinct strains were identified based on the size and extent of these inserts. One strain comprised two small inserts of foreign DNA up- and downstream of <i>oriC</i>; one of about 7000 nt or 0.25% originated from CC692 and the other, at ca. 38,000 nt or 1.3% slightly larger one was of CC522 provenance. The second strain carried a larger CC692 insert (nearly 257,000 nt or 10% of the strain’s genome), and its CC522-derived insert was also larger, at about 53,500 nt or 2% of the genome). The third strain carried an identical CC692-derived region (in which the same mutations were observed as in the second strain), but it had a considerably larger CC522-like insertion of about 167,000 nt or 5.9% of the genome. Both isolates of the first, and two out of four isolates of the second strain also harbored a hemolysin-beta-integrating prophage carrying “bird-specific” virulence factors, ornithine cyclodeaminase D0K6J8 and a putative protease D0K6J9. Furthermore, isolates had two different variants of SCC elements that lacked <i>mecA/mecC</i> genes. These findings highlight the role of horizontal gene transfer in the evolution of <i>S. aureus</i> facilitated by SCC elements, by phages, and by a yet undescribed mechanism for large-scale exchange of core genomic DNA. |
| first_indexed | 2024-03-08T09:51:19Z |
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| id | doaj.art-cd6cf544f51e431ea3ac115091fa12fa |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-08T09:51:19Z |
| publishDate | 2024-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-cd6cf544f51e431ea3ac115091fa12fa2024-01-29T14:06:14ZengMDPI AGMicroorganisms2076-26072024-01-011219610.3390/microorganisms12010096Molecular Characterization of Chimeric <i>Staphylococcus aureus</i> Strains from WaterfowlStefan Monecke0Sascha D. Braun1Maximillian Collatz2Celia Diezel3Elke Müller4Martin Reinicke5Adriana Cabal Rosel6Andrea T. Feßler7Dennis Hanke8Igor Loncaric9Stefan Schwarz10Sonia Cortez de Jäckel11Werner Ruppitsch12Dolores Gavier-Widén13Helmut Hotzel14Ralf Ehricht15Leibniz Institute of Photonic Technology (IPHT), Leibniz Center for Photonics in Infection Research (LPI), 07745 Jena, GermanyLeibniz Institute of Photonic Technology (IPHT), Leibniz Center for Photonics in Infection Research (LPI), 07745 Jena, GermanyLeibniz Institute of Photonic Technology (IPHT), Leibniz Center for Photonics in Infection Research (LPI), 07745 Jena, GermanyLeibniz Institute of Photonic Technology (IPHT), Leibniz Center for Photonics in Infection Research (LPI), 07745 Jena, GermanyLeibniz Institute of Photonic Technology (IPHT), Leibniz Center for Photonics in Infection Research (LPI), 07745 Jena, GermanyLeibniz Institute of Photonic Technology (IPHT), Leibniz Center for Photonics in Infection Research (LPI), 07745 Jena, GermanyAustrian Agency for Health and Food Safety, Institute for Medical Microbiology and Hygiene, 1220 Vienna, AustriaInstitute of Microbiology and Epizootics, Centre for Infection, Medicine School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, GermanyInstitute of Microbiology and Epizootics, Centre for Infection, Medicine School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, GermanyInstitute of Microbiology, University of Veterinary Medicine, 1210 Vienna, AustriaInstitute of Microbiology and Epizootics, Centre for Infection, Medicine School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, GermanyPoultry Clinics and Laboratory Pöppel, 33129 Delbrück, GermanyAustrian Agency for Health and Food Safety, Institute for Medical Microbiology and Hygiene, 1220 Vienna, AustriaDepartment of Pathology and Wildlife Disease, National Veterinary Institute (SVA), 75189 Uppsala, SwedenInstitute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut (Federal Research Institute for Animal Health), 07743 Jena, GermanyLeibniz Institute of Photonic Technology (IPHT), Leibniz Center for Photonics in Infection Research (LPI), 07745 Jena, Germany<i>Staphylococcus aureus</i> is a versatile pathogen that does not only occur in humans but also in various wild and domestic animals, including several avian species. When characterizing <i>S. aureus</i> isolates from waterfowl, isolates were identified as atypical CC133 by DNA microarray analysis. They differed from previously sequenced CC133 strains in the presence of the collagen adhesin gene <i>cna</i>; some also showed a different capsule type and a deviant <i>spa</i> type. Thus, they were subjected to whole-genome sequencing. This revealed multiple insertions of large regions of DNA from other <i>S. aureus</i> lineages into a CC133-derived backbone genome. Three distinct strains were identified based on the size and extent of these inserts. One strain comprised two small inserts of foreign DNA up- and downstream of <i>oriC</i>; one of about 7000 nt or 0.25% originated from CC692 and the other, at ca. 38,000 nt or 1.3% slightly larger one was of CC522 provenance. The second strain carried a larger CC692 insert (nearly 257,000 nt or 10% of the strain’s genome), and its CC522-derived insert was also larger, at about 53,500 nt or 2% of the genome). The third strain carried an identical CC692-derived region (in which the same mutations were observed as in the second strain), but it had a considerably larger CC522-like insertion of about 167,000 nt or 5.9% of the genome. Both isolates of the first, and two out of four isolates of the second strain also harbored a hemolysin-beta-integrating prophage carrying “bird-specific” virulence factors, ornithine cyclodeaminase D0K6J8 and a putative protease D0K6J9. Furthermore, isolates had two different variants of SCC elements that lacked <i>mecA/mecC</i> genes. These findings highlight the role of horizontal gene transfer in the evolution of <i>S. aureus</i> facilitated by SCC elements, by phages, and by a yet undescribed mechanism for large-scale exchange of core genomic DNA.https://www.mdpi.com/2076-2607/12/1/96<i>Staphylococcus aureus</i>clonal complex 133clonal complex 522clonal complex 692next generation sequencingbacteriophages |
| spellingShingle | Stefan Monecke Sascha D. Braun Maximillian Collatz Celia Diezel Elke Müller Martin Reinicke Adriana Cabal Rosel Andrea T. Feßler Dennis Hanke Igor Loncaric Stefan Schwarz Sonia Cortez de Jäckel Werner Ruppitsch Dolores Gavier-Widén Helmut Hotzel Ralf Ehricht Molecular Characterization of Chimeric <i>Staphylococcus aureus</i> Strains from Waterfowl Microorganisms <i>Staphylococcus aureus</i> clonal complex 133 clonal complex 522 clonal complex 692 next generation sequencing bacteriophages |
| title | Molecular Characterization of Chimeric <i>Staphylococcus aureus</i> Strains from Waterfowl |
| title_full | Molecular Characterization of Chimeric <i>Staphylococcus aureus</i> Strains from Waterfowl |
| title_fullStr | Molecular Characterization of Chimeric <i>Staphylococcus aureus</i> Strains from Waterfowl |
| title_full_unstemmed | Molecular Characterization of Chimeric <i>Staphylococcus aureus</i> Strains from Waterfowl |
| title_short | Molecular Characterization of Chimeric <i>Staphylococcus aureus</i> Strains from Waterfowl |
| title_sort | molecular characterization of chimeric i staphylococcus aureus i strains from waterfowl |
| topic | <i>Staphylococcus aureus</i> clonal complex 133 clonal complex 522 clonal complex 692 next generation sequencing bacteriophages |
| url | https://www.mdpi.com/2076-2607/12/1/96 |
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