Characterisation of <i>Staphylococcus aureus</i> Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes <i>lukP/Q</i>

Leukocidins of <i>Staphylococcus</i> (<i>S</i>.) <i>aureus</i> are bicomponent toxins that form polymeric pores in host leukocyte membranes, leading to cell death and/or triggering apoptosis. Some of these toxin genes are located on prophages and are associated wi...

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Main Authors: Stefan Monecke, Sindy Burgold-Voigt, Andrea T. Feßler, Martina Krapf, Igor Loncaric, Elisabeth M. Liebler-Tenorio, Sascha D. Braun, Celia Diezel, Elke Müller, Martin Reinicke, Annett Reissig, Adriana Cabal Rosel, Werner Ruppitsch, Helmut Hotzel, Dennis Hanke, Christiane Cuny, Wolfgang Witte, Stefan Schwarz, Ralf Ehricht
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Language:English
Published: MDPI AG 2025-01-01
Series:Toxins
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Online Access:https://www.mdpi.com/2072-6651/17/1/20
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author Stefan Monecke
Sindy Burgold-Voigt
Andrea T. Feßler
Martina Krapf
Igor Loncaric
Elisabeth M. Liebler-Tenorio
Sascha D. Braun
Celia Diezel
Elke Müller
Martin Reinicke
Annett Reissig
Adriana Cabal Rosel
Werner Ruppitsch
Helmut Hotzel
Dennis Hanke
Christiane Cuny
Wolfgang Witte
Stefan Schwarz
Ralf Ehricht
author_facet Stefan Monecke
Sindy Burgold-Voigt
Andrea T. Feßler
Martina Krapf
Igor Loncaric
Elisabeth M. Liebler-Tenorio
Sascha D. Braun
Celia Diezel
Elke Müller
Martin Reinicke
Annett Reissig
Adriana Cabal Rosel
Werner Ruppitsch
Helmut Hotzel
Dennis Hanke
Christiane Cuny
Wolfgang Witte
Stefan Schwarz
Ralf Ehricht
author_sort Stefan Monecke
collection DOAJ
description Leukocidins of <i>Staphylococcus</i> (<i>S</i>.) <i>aureus</i> are bicomponent toxins that form polymeric pores in host leukocyte membranes, leading to cell death and/or triggering apoptosis. Some of these toxin genes are located on prophages and are associated with specific hosts. The genes <i>lukP/Q</i> have been described from equine <i>S. aureus</i> isolates. We examined the genomes, including the <i>lukP/Q</i> prophages, of <i>S. aureus</i> strains belonging to clonal complexes CC1, CC350, CC816, and CC8115. In addition to sequencing, phages were characterised by mitomycin C induction and transmission electron microscopy (TEM). All <i>lukP/Q</i> prophages integrated into the <i>lip2</i>=<i>geh</i> gene, and all included also the gene <i>scn-eq</i> encoding an equine staphylococcal complement inhibitor. The <i>lukP/Q</i> prophages clustered, based on gene content and allelic variants, into three groups. One was found in CC1 and CC97 sequences; one was present mainly in CC350 but also in other lineages (CC1, CC97, CC133, CC398); and a third one was exclusively observed in CC816 and CC8115. Prophages of the latter group additionally included a rare enterotoxin A allele (<i>sea</i><sub>320E</sub>). Moreover, a prophage from a CC522 goat isolate was found to harbour <i>lukP</i>. Its <i>lukF</i> component could be regarded as chimaera comprising parts of <i>lukQ</i> and of <i>lukF-P83</i>. A putative kinase gene of 1095 basepairs was found to be associated with equine strains of <i>S. aureus</i>. It was also localised on prophages. However, these prophages were different from the ones that carried <i>lukP/Q</i>, and three different integration sites of kinase-carrying phages were identified. These observations confirmed the presence of prophage-located important virulence-associated genes in equine <i>S. aureus</i> and that certain prophages might determine the host specificity of the staphylococcal strains they reside in.
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spelling doaj-art-ed206d1b151b4b1d9a6e03e90c5f7e012025-01-24T13:51:13ZengMDPI AGToxins2072-66512025-01-011712010.3390/toxins17010020Characterisation of <i>Staphylococcus aureus</i> Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes <i>lukP/Q</i>Stefan Monecke0Sindy Burgold-Voigt1Andrea T. Feßler2Martina Krapf3Igor Loncaric4Elisabeth M. Liebler-Tenorio5Sascha D. Braun6Celia Diezel7Elke Müller8Martin Reinicke9Annett Reissig10Adriana Cabal Rosel11Werner Ruppitsch12Helmut Hotzel13Dennis Hanke14Christiane Cuny15Wolfgang Witte16Stefan Schwarz17Ralf Ehricht18Leibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, GermanyLeibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, GermanyInstitute of Microbiology and Epizootics and Veterinary Centre for Resistance Research (TZR), School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, GermanyLABOKLIN GmbH&Co. KG, 97688 Bad Kissingen, GermanyInstitute of Microbiology, University of Veterinary Medicine Vienna, 1210 Vienna, AustriaInstitute of Molecular Pathogenesis, Friedrich-Loeffler-Institute (Federal Research Institute for Animal Health), 07743 Jena, GermanyLeibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, GermanyLeibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, GermanyLeibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, GermanyLeibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, GermanyLeibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, GermanyAustrian Agency for Health and Food Safety (AGES), Institute for Medical Microbiology and Hygiene, 1090 Vienna, AustriaAustrian Agency for Health and Food Safety (AGES), Institute for Medical Microbiology and Hygiene, 1090 Vienna, AustriaInstitute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institute (Federal Research Institute for Animal Health), 07743 Jena, GermanyInstitute of Microbiology and Epizootics and Veterinary Centre for Resistance Research (TZR), School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, GermanyRobert Koch Institute, Wernigerode Branch, 38855 Wernigerode, GermanyRobert Koch Institute, Wernigerode Branch, 38855 Wernigerode, GermanyInstitute of Microbiology and Epizootics and Veterinary Centre for Resistance Research (TZR), School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, GermanyLeibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, GermanyLeukocidins of <i>Staphylococcus</i> (<i>S</i>.) <i>aureus</i> are bicomponent toxins that form polymeric pores in host leukocyte membranes, leading to cell death and/or triggering apoptosis. Some of these toxin genes are located on prophages and are associated with specific hosts. The genes <i>lukP/Q</i> have been described from equine <i>S. aureus</i> isolates. We examined the genomes, including the <i>lukP/Q</i> prophages, of <i>S. aureus</i> strains belonging to clonal complexes CC1, CC350, CC816, and CC8115. In addition to sequencing, phages were characterised by mitomycin C induction and transmission electron microscopy (TEM). All <i>lukP/Q</i> prophages integrated into the <i>lip2</i>=<i>geh</i> gene, and all included also the gene <i>scn-eq</i> encoding an equine staphylococcal complement inhibitor. The <i>lukP/Q</i> prophages clustered, based on gene content and allelic variants, into three groups. One was found in CC1 and CC97 sequences; one was present mainly in CC350 but also in other lineages (CC1, CC97, CC133, CC398); and a third one was exclusively observed in CC816 and CC8115. Prophages of the latter group additionally included a rare enterotoxin A allele (<i>sea</i><sub>320E</sub>). Moreover, a prophage from a CC522 goat isolate was found to harbour <i>lukP</i>. Its <i>lukF</i> component could be regarded as chimaera comprising parts of <i>lukQ</i> and of <i>lukF-P83</i>. A putative kinase gene of 1095 basepairs was found to be associated with equine strains of <i>S. aureus</i>. It was also localised on prophages. However, these prophages were different from the ones that carried <i>lukP/Q</i>, and three different integration sites of kinase-carrying phages were identified. These observations confirmed the presence of prophage-located important virulence-associated genes in equine <i>S. aureus</i> and that certain prophages might determine the host specificity of the staphylococcal strains they reside in.https://www.mdpi.com/2072-6651/17/1/20<i>Staphylococcus aureus</i>leukocidinsprophagesbacteriophages<i>lukP/Q</i>horse (<i>Equus caballus</i>)
spellingShingle Stefan Monecke
Sindy Burgold-Voigt
Andrea T. Feßler
Martina Krapf
Igor Loncaric
Elisabeth M. Liebler-Tenorio
Sascha D. Braun
Celia Diezel
Elke Müller
Martin Reinicke
Annett Reissig
Adriana Cabal Rosel
Werner Ruppitsch
Helmut Hotzel
Dennis Hanke
Christiane Cuny
Wolfgang Witte
Stefan Schwarz
Ralf Ehricht
Characterisation of <i>Staphylococcus aureus</i> Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes <i>lukP/Q</i>
Toxins
<i>Staphylococcus aureus</i>
leukocidins
prophages
bacteriophages
<i>lukP/Q</i>
horse (<i>Equus caballus</i>)
title Characterisation of <i>Staphylococcus aureus</i> Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes <i>lukP/Q</i>
title_full Characterisation of <i>Staphylococcus aureus</i> Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes <i>lukP/Q</i>
title_fullStr Characterisation of <i>Staphylococcus aureus</i> Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes <i>lukP/Q</i>
title_full_unstemmed Characterisation of <i>Staphylococcus aureus</i> Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes <i>lukP/Q</i>
title_short Characterisation of <i>Staphylococcus aureus</i> Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes <i>lukP/Q</i>
title_sort characterisation of i staphylococcus aureus i strains and their prophages that carry horse specific leukocidin genes i lukp q i
topic <i>Staphylococcus aureus</i>
leukocidins
prophages
bacteriophages
<i>lukP/Q</i>
horse (<i>Equus caballus</i>)
url https://www.mdpi.com/2072-6651/17/1/20
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