Origin and Evolution of European Community-Acquired Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content>
ABSTRACT Community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) was recognized in Europe and worldwide in the late 1990s. Within a decade, several genetically and geographically distinct CA-MRSA lineages carrying the small SCCmec type IV and V genetic elements and the Panton-Valent...
Guardado en:
| Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Formato: | article |
| Lenguaje: | EN |
| Publicado: |
American Society for Microbiology
2014
|
| Materias: | |
| Acceso en línea: | https://doaj.org/article/f59177fc13fe4f059add8a143959b6d5 |
| Etiquetas: |
Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
|
| id |
oai:doaj.org-article:f59177fc13fe4f059add8a143959b6d5 |
|---|---|
| record_format |
dspace |
| spelling |
oai:doaj.org-article:f59177fc13fe4f059add8a143959b6d52021-11-15T15:45:54ZOrigin and Evolution of European Community-Acquired Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content>10.1128/mBio.01044-142150-7511https://doaj.org/article/f59177fc13fe4f059add8a143959b6d52014-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01044-14https://doaj.org/toc/2150-7511ABSTRACT Community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) was recognized in Europe and worldwide in the late 1990s. Within a decade, several genetically and geographically distinct CA-MRSA lineages carrying the small SCCmec type IV and V genetic elements and the Panton-Valentine leukocidin (PVL) emerged around the world. In Europe, the predominant CA-MRSA strain belongs to clonal complex 80 (CC80) and is resistant to kanamycin/amikacin and fusidic acid. CC80 was first reported in 1993 but was relatively rare until the late 1990s. It has since been identified throughout North Africa, the Middle East, and Europe, with recent sporadic reports in sub-Saharan Africa. While strongly associated with skin and soft tissue infections, it is rarely found among asymptomatic carriers. Methicillin-sensitive S. aureus (MSSA) CC80 strains are extremely rare except in sub-Saharan Africa. In the current study, we applied whole-genome sequencing to a global collection of both MSSA and MRSA CC80 isolates. Phylogenetic analyses strongly suggest that the European epidemic CA-MRSA lineage is derived from a PVL-positive MSSA ancestor from sub-Saharan Africa. Moreover, the tree topology suggests a single acquisition of both the SCCmec element and a plasmid encoding the fusidic acid resistance determinant. Four canonical SNPs distinguish the derived CA-MRSA lineage and include a nonsynonymous mutation in accessory gene regulator C (agrC). These changes were associated with a star-like expansion into Europe, the Middle East, and North Africa in the early 1990s, including multiple cases of cross-continent imports likely driven by human migrations. IMPORTANCE With increasing levels of CA-MRSA reported from most parts of the Western world, there is a great interest in understanding the origin and factors associated with the emergence of these epidemic lineages. To trace the origin, evolution, and dissemination pattern of the European CA-MRSA clone (CC80), we sequenced a global collection of strains of the S. aureus CC80 lineage. Our study determined that a single descendant of a PVL-positive methicillin-sensitive ancestor circulating in sub-Saharan Africa rose to become the dominant CA-MRSA clone in Europe, the Middle East, and North Africa. In the transition from a methicillin-susceptible lineage to a successful CA-MRSA clone, it simultaneously became resistant to fusidic acid, a widely used antibiotic for skin and soft tissue infections, thus demonstrating the importance of antibiotic selection in the success of this clone. This finding furthermore highlights the significance of horizontal gene acquisitions and underscores the combined importance of these factors for the success of CA-MRSA.Marc SteggerThierry WirthPaal S. AndersenRobert L. SkovAnna De GrassiPatricia Martins SimõesAnne TristanAndreas PetersenMaliha AzizKristoffer KiilIvana CirkovićEdet E. UdoRosa del CampoJaana Vuopio-VarkilaNorazah AhmadSima TokajianGeorg PetersFrieder SchaumburgBarbro Olsson-LiljequistMichael GivskovElizabeth E. DriebeHenrik E. VighAdebayo ShittuNadjia Ramdani-BougessaJean-Philippe RasigadeLance B. PriceFrancois VandeneschAnders R. LarsenFrederic LaurentAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 5 (2014) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Microbiology QR1-502 |
| spellingShingle |
Microbiology QR1-502 Marc Stegger Thierry Wirth Paal S. Andersen Robert L. Skov Anna De Grassi Patricia Martins Simões Anne Tristan Andreas Petersen Maliha Aziz Kristoffer Kiil Ivana Cirković Edet E. Udo Rosa del Campo Jaana Vuopio-Varkila Norazah Ahmad Sima Tokajian Georg Peters Frieder Schaumburg Barbro Olsson-Liljequist Michael Givskov Elizabeth E. Driebe Henrik E. Vigh Adebayo Shittu Nadjia Ramdani-Bougessa Jean-Philippe Rasigade Lance B. Price Francois Vandenesch Anders R. Larsen Frederic Laurent Origin and Evolution of European Community-Acquired Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| description |
ABSTRACT Community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) was recognized in Europe and worldwide in the late 1990s. Within a decade, several genetically and geographically distinct CA-MRSA lineages carrying the small SCCmec type IV and V genetic elements and the Panton-Valentine leukocidin (PVL) emerged around the world. In Europe, the predominant CA-MRSA strain belongs to clonal complex 80 (CC80) and is resistant to kanamycin/amikacin and fusidic acid. CC80 was first reported in 1993 but was relatively rare until the late 1990s. It has since been identified throughout North Africa, the Middle East, and Europe, with recent sporadic reports in sub-Saharan Africa. While strongly associated with skin and soft tissue infections, it is rarely found among asymptomatic carriers. Methicillin-sensitive S. aureus (MSSA) CC80 strains are extremely rare except in sub-Saharan Africa. In the current study, we applied whole-genome sequencing to a global collection of both MSSA and MRSA CC80 isolates. Phylogenetic analyses strongly suggest that the European epidemic CA-MRSA lineage is derived from a PVL-positive MSSA ancestor from sub-Saharan Africa. Moreover, the tree topology suggests a single acquisition of both the SCCmec element and a plasmid encoding the fusidic acid resistance determinant. Four canonical SNPs distinguish the derived CA-MRSA lineage and include a nonsynonymous mutation in accessory gene regulator C (agrC). These changes were associated with a star-like expansion into Europe, the Middle East, and North Africa in the early 1990s, including multiple cases of cross-continent imports likely driven by human migrations. IMPORTANCE With increasing levels of CA-MRSA reported from most parts of the Western world, there is a great interest in understanding the origin and factors associated with the emergence of these epidemic lineages. To trace the origin, evolution, and dissemination pattern of the European CA-MRSA clone (CC80), we sequenced a global collection of strains of the S. aureus CC80 lineage. Our study determined that a single descendant of a PVL-positive methicillin-sensitive ancestor circulating in sub-Saharan Africa rose to become the dominant CA-MRSA clone in Europe, the Middle East, and North Africa. In the transition from a methicillin-susceptible lineage to a successful CA-MRSA clone, it simultaneously became resistant to fusidic acid, a widely used antibiotic for skin and soft tissue infections, thus demonstrating the importance of antibiotic selection in the success of this clone. This finding furthermore highlights the significance of horizontal gene acquisitions and underscores the combined importance of these factors for the success of CA-MRSA. |
| format |
article |
| author |
Marc Stegger Thierry Wirth Paal S. Andersen Robert L. Skov Anna De Grassi Patricia Martins Simões Anne Tristan Andreas Petersen Maliha Aziz Kristoffer Kiil Ivana Cirković Edet E. Udo Rosa del Campo Jaana Vuopio-Varkila Norazah Ahmad Sima Tokajian Georg Peters Frieder Schaumburg Barbro Olsson-Liljequist Michael Givskov Elizabeth E. Driebe Henrik E. Vigh Adebayo Shittu Nadjia Ramdani-Bougessa Jean-Philippe Rasigade Lance B. Price Francois Vandenesch Anders R. Larsen Frederic Laurent |
| author_facet |
Marc Stegger Thierry Wirth Paal S. Andersen Robert L. Skov Anna De Grassi Patricia Martins Simões Anne Tristan Andreas Petersen Maliha Aziz Kristoffer Kiil Ivana Cirković Edet E. Udo Rosa del Campo Jaana Vuopio-Varkila Norazah Ahmad Sima Tokajian Georg Peters Frieder Schaumburg Barbro Olsson-Liljequist Michael Givskov Elizabeth E. Driebe Henrik E. Vigh Adebayo Shittu Nadjia Ramdani-Bougessa Jean-Philippe Rasigade Lance B. Price Francois Vandenesch Anders R. Larsen Frederic Laurent |
| author_sort |
Marc Stegger |
| title |
Origin and Evolution of European Community-Acquired Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_short |
Origin and Evolution of European Community-Acquired Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_full |
Origin and Evolution of European Community-Acquired Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_fullStr |
Origin and Evolution of European Community-Acquired Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_full_unstemmed |
Origin and Evolution of European Community-Acquired Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_sort |
origin and evolution of european community-acquired methicillin-resistant <named-content content-type="genus-species">staphylococcus aureus</named-content> |
| publisher |
American Society for Microbiology |
| publishDate |
2014 |
| url |
https://doaj.org/article/f59177fc13fe4f059add8a143959b6d5 |
| work_keys_str_mv |
AT marcstegger originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT thierrywirth originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT paalsandersen originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT robertlskov originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT annadegrassi originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT patriciamartinssimoes originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT annetristan originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT andreaspetersen originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT malihaaziz originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT kristofferkiil originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT ivanacirkovic originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT edeteudo originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT rosadelcampo originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT jaanavuopiovarkila originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT norazahahmad originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT simatokajian originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT georgpeters originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT friederschaumburg originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT barbroolssonliljequist originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT michaelgivskov originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT elizabethedriebe originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT henrikevigh originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT adebayoshittu originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT nadjiaramdanibougessa originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT jeanphilipperasigade originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT lancebprice originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT francoisvandenesch originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT andersrlarsen originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT fredericlaurent originandevolutionofeuropeancommunityacquiredmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent |
| _version_ |
1718427559156252672 |