Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 Lineage
Until 2007, Staphylococcus aureus from clonal complex 398 (CC398) was exclusively associated with livestock species and companion animals. Recently, several studies described the emergence of S. aureus CC398 as etiologies of severe infections in humans living in an animal-free environment. Recent se...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-04-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.00742/full |
| _version_ | 1818924505428393984 |
|---|---|
| author | Floriane Laumay Anna-Rita Corvaglia Seydina M. Diene Myriam Girard Frank Oechslin Nathalie van der Mee-Marquet José Manuel Entenza Patrice François |
| author_facet | Floriane Laumay Anna-Rita Corvaglia Seydina M. Diene Myriam Girard Frank Oechslin Nathalie van der Mee-Marquet José Manuel Entenza Patrice François |
| author_sort | Floriane Laumay |
| collection | DOAJ |
| description | Until 2007, Staphylococcus aureus from clonal complex 398 (CC398) was exclusively associated with livestock species and companion animals. Recently, several studies described the emergence of S. aureus CC398 as etiologies of severe infections in humans living in an animal-free environment. Recent sequencing efforts showed that the mobile genetic elements found in CC398 isolates were specific for each population and enabled differentiation of strains responsible for asymptomatic colonization from strains involved in bloodstream infections. We mobilized prophages from a human CC398 isolate and introduced them into two naïve ancestral isolates devoid of prophages that exclusively colonize animals. These lysogenized ancestral CC398 isolates acquired features related to virulence, such as an increased capacity to adhere to human extracellular matrix proteins and the ability to invade and survive within non-phagocytic cells. Pathogenicity of several clinical isolates from the CC398 lineage as well as ancestral and in vitro lysogenized ancestral counterparts was assessed in a model of infectious endocarditis in rats. Natural and artificial lysogens were not only more invasive than their prophage-free parent but also showed an increased capacity to multiply within aortic vegetations. This study identified prophages as mediators of bacterial virulence in a model of infectious endocarditis, probably through promotion of interaction with extracellular matrix components. Further studies are needed to identify mechanisms leading to promotion of intrinsic virulence. |
| first_indexed | 2024-12-20T02:26:24Z |
| format | Article |
| id | doaj.art-09ed5d5ef8f04dd49f4ac7a7d5dbb856 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-20T02:26:24Z |
| publishDate | 2019-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-09ed5d5ef8f04dd49f4ac7a7d5dbb8562022-12-21T19:56:41ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-04-011010.3389/fmicb.2019.00742446881Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 LineageFloriane Laumay0Anna-Rita Corvaglia1Seydina M. Diene2Myriam Girard3Frank Oechslin4Nathalie van der Mee-Marquet5José Manuel Entenza6Patrice François7Genomic Research Laboratory, Service of Infectious Diseases, Medical University Center, Geneva University Hospitals, Geneva, SwitzerlandGenomic Research Laboratory, Service of Infectious Diseases, Medical University Center, Geneva University Hospitals, Geneva, SwitzerlandUnité de Recherche sur les Maladies Infectieuses et Tropicales Émergentes, Faculté de Médecine et de Pharmacie, Aix-Marseille University, Marseille, FranceGenomic Research Laboratory, Service of Infectious Diseases, Medical University Center, Geneva University Hospitals, Geneva, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandUMR 1282 Infectiologie Santé Publique, Université de Tours, Tours, FranceDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandGenomic Research Laboratory, Service of Infectious Diseases, Medical University Center, Geneva University Hospitals, Geneva, SwitzerlandUntil 2007, Staphylococcus aureus from clonal complex 398 (CC398) was exclusively associated with livestock species and companion animals. Recently, several studies described the emergence of S. aureus CC398 as etiologies of severe infections in humans living in an animal-free environment. Recent sequencing efforts showed that the mobile genetic elements found in CC398 isolates were specific for each population and enabled differentiation of strains responsible for asymptomatic colonization from strains involved in bloodstream infections. We mobilized prophages from a human CC398 isolate and introduced them into two naïve ancestral isolates devoid of prophages that exclusively colonize animals. These lysogenized ancestral CC398 isolates acquired features related to virulence, such as an increased capacity to adhere to human extracellular matrix proteins and the ability to invade and survive within non-phagocytic cells. Pathogenicity of several clinical isolates from the CC398 lineage as well as ancestral and in vitro lysogenized ancestral counterparts was assessed in a model of infectious endocarditis in rats. Natural and artificial lysogens were not only more invasive than their prophage-free parent but also showed an increased capacity to multiply within aortic vegetations. This study identified prophages as mediators of bacterial virulence in a model of infectious endocarditis, probably through promotion of interaction with extracellular matrix components. Further studies are needed to identify mechanisms leading to promotion of intrinsic virulence.https://www.frontiersin.org/article/10.3389/fmicb.2019.00742/fullStaphylococcus aureusbacteriophages (phages)virulenceinfectionadhesioninternalization |
| spellingShingle | Floriane Laumay Anna-Rita Corvaglia Seydina M. Diene Myriam Girard Frank Oechslin Nathalie van der Mee-Marquet José Manuel Entenza Patrice François Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 Lineage Frontiers in Microbiology Staphylococcus aureus bacteriophages (phages) virulence infection adhesion internalization |
| title | Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 Lineage |
| title_full | Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 Lineage |
| title_fullStr | Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 Lineage |
| title_full_unstemmed | Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 Lineage |
| title_short | Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 Lineage |
| title_sort | temperate prophages increase bacterial adhesin expression and virulence in an experimental model of endocarditis due to staphylococcus aureus from the cc398 lineage |
| topic | Staphylococcus aureus bacteriophages (phages) virulence infection adhesion internalization |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.00742/full |
| work_keys_str_mv | AT florianelaumay temperateprophagesincreasebacterialadhesinexpressionandvirulenceinanexperimentalmodelofendocarditisduetostaphylococcusaureusfromthecc398lineage AT annaritacorvaglia temperateprophagesincreasebacterialadhesinexpressionandvirulenceinanexperimentalmodelofendocarditisduetostaphylococcusaureusfromthecc398lineage AT seydinamdiene temperateprophagesincreasebacterialadhesinexpressionandvirulenceinanexperimentalmodelofendocarditisduetostaphylococcusaureusfromthecc398lineage AT myriamgirard temperateprophagesincreasebacterialadhesinexpressionandvirulenceinanexperimentalmodelofendocarditisduetostaphylococcusaureusfromthecc398lineage AT frankoechslin temperateprophagesincreasebacterialadhesinexpressionandvirulenceinanexperimentalmodelofendocarditisduetostaphylococcusaureusfromthecc398lineage AT nathalievandermeemarquet temperateprophagesincreasebacterialadhesinexpressionandvirulenceinanexperimentalmodelofendocarditisduetostaphylococcusaureusfromthecc398lineage AT josemanuelentenza temperateprophagesincreasebacterialadhesinexpressionandvirulenceinanexperimentalmodelofendocarditisduetostaphylococcusaureusfromthecc398lineage AT patricefrancois temperateprophagesincreasebacterialadhesinexpressionandvirulenceinanexperimentalmodelofendocarditisduetostaphylococcusaureusfromthecc398lineage |