<named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock
ABSTRACT Since its discovery in the early 2000s, methicillin-resistant Staphylococcus aureus (MRSA) clonal complex 398 (CC398) has become a rapidly emerging cause of human infections, most often associated with livestock exposure. We applied whole-genome sequence typing to characterize a diverse col...
Guardado en:
| Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Formato: | article |
| Lenguaje: | EN |
| Publicado: |
American Society for Microbiology
2012
|
| Materias: | |
| Acceso en línea: | https://doaj.org/article/b9fabdb17e9740f3b86c452ad4ee246a |
| Etiquetas: |
Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
|
| id |
oai:doaj.org-article:b9fabdb17e9740f3b86c452ad4ee246a |
|---|---|
| record_format |
dspace |
| spelling |
oai:doaj.org-article:b9fabdb17e9740f3b86c452ad4ee246a2021-11-15T15:39:02Z<named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock10.1128/mBio.00305-112150-7511https://doaj.org/article/b9fabdb17e9740f3b86c452ad4ee246a2012-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00305-11https://doaj.org/toc/2150-7511ABSTRACT Since its discovery in the early 2000s, methicillin-resistant Staphylococcus aureus (MRSA) clonal complex 398 (CC398) has become a rapidly emerging cause of human infections, most often associated with livestock exposure. We applied whole-genome sequence typing to characterize a diverse collection of CC398 isolates (n = 89), including MRSA and methicillin-susceptible S. aureus (MSSA) from animals and humans spanning 19 countries and four continents. We identified 4,238 single nucleotide polymorphisms (SNPs) among the 89 core genomes. Minimal homoplasy (consistency index = 0.9591) was detected among parsimony-informative SNPs, allowing for the generation of a highly accurate phylogenetic reconstruction of the CC398 clonal lineage. Phylogenetic analyses revealed that MSSA from humans formed the most ancestral clades. The most derived lineages were composed predominantly of livestock-associated MRSA possessing three different staphylococcal cassette chromosome mec element (SCCmec) types (IV, V, and VII-like) including nine subtypes. The human-associated isolates from the basal clades carried phages encoding human innate immune modulators that were largely missing among the livestock-associated isolates. Our results strongly suggest that livestock-associated MRSA CC398 originated in humans as MSSA. The lineage appears to have undergone a rapid radiation in conjunction with the jump from humans to livestock, where it subsequently acquired tetracycline and methicillin resistance. Further analyses are required to estimate the number of independent genetic events leading to the methicillin-resistant sublineages, but the diversity of SCCmec subtypes is suggestive of strong and diverse antimicrobial selection associated with food animal production. IMPORTANCE Modern food animal production is characterized by densely concentrated animals and routine antibiotic use, which may facilitate the emergence of novel antibiotic-resistant zoonotic pathogens. Our findings strongly support the idea that livestock-associated MRSA CC398 originated as MSSA in humans. The jump of CC398 from humans to livestock was accompanied by the loss of phage-carried human virulence genes, which likely attenuated its zoonotic potential, but it was also accompanied by the acquisition of tetracycline and methicillin resistance. Our findings exemplify a bidirectional zoonotic exchange and underscore the potential public health risks of widespread antibiotic use in food animal production.Lance B. PriceMarc SteggerHenrik HasmanMaliha AzizJesper LarsenPaal Skytt AndersenTalima PearsonAndrew E. WatersJeffrey T. FosterJames SchuppJohn GilleceElizabeth DriebeCindy M. LiuBurkhard SpringerIrena ZdovcAntonio BattistiAlessia FrancoJacek ŻmudzkiStefan SchwarzPatrick ButayeEric JouyConstanca PombaM. Concepción PorreroRaymond RuimyTara C. SmithD. Ashley RobinsonJ. Scott WeeseCarmen Sofia ArriolaFangyou YuFrederic LaurentPaul KeimRobert SkovFrank M. AarestrupAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 1 (2012) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Microbiology QR1-502 |
| spellingShingle |
Microbiology QR1-502 Lance B. Price Marc Stegger Henrik Hasman Maliha Aziz Jesper Larsen Paal Skytt Andersen Talima Pearson Andrew E. Waters Jeffrey T. Foster James Schupp John Gillece Elizabeth Driebe Cindy M. Liu Burkhard Springer Irena Zdovc Antonio Battisti Alessia Franco Jacek Żmudzki Stefan Schwarz Patrick Butaye Eric Jouy Constanca Pomba M. Concepción Porrero Raymond Ruimy Tara C. Smith D. Ashley Robinson J. Scott Weese Carmen Sofia Arriola Fangyou Yu Frederic Laurent Paul Keim Robert Skov Frank M. Aarestrup <named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock |
| description |
ABSTRACT Since its discovery in the early 2000s, methicillin-resistant Staphylococcus aureus (MRSA) clonal complex 398 (CC398) has become a rapidly emerging cause of human infections, most often associated with livestock exposure. We applied whole-genome sequence typing to characterize a diverse collection of CC398 isolates (n = 89), including MRSA and methicillin-susceptible S. aureus (MSSA) from animals and humans spanning 19 countries and four continents. We identified 4,238 single nucleotide polymorphisms (SNPs) among the 89 core genomes. Minimal homoplasy (consistency index = 0.9591) was detected among parsimony-informative SNPs, allowing for the generation of a highly accurate phylogenetic reconstruction of the CC398 clonal lineage. Phylogenetic analyses revealed that MSSA from humans formed the most ancestral clades. The most derived lineages were composed predominantly of livestock-associated MRSA possessing three different staphylococcal cassette chromosome mec element (SCCmec) types (IV, V, and VII-like) including nine subtypes. The human-associated isolates from the basal clades carried phages encoding human innate immune modulators that were largely missing among the livestock-associated isolates. Our results strongly suggest that livestock-associated MRSA CC398 originated in humans as MSSA. The lineage appears to have undergone a rapid radiation in conjunction with the jump from humans to livestock, where it subsequently acquired tetracycline and methicillin resistance. Further analyses are required to estimate the number of independent genetic events leading to the methicillin-resistant sublineages, but the diversity of SCCmec subtypes is suggestive of strong and diverse antimicrobial selection associated with food animal production. IMPORTANCE Modern food animal production is characterized by densely concentrated animals and routine antibiotic use, which may facilitate the emergence of novel antibiotic-resistant zoonotic pathogens. Our findings strongly support the idea that livestock-associated MRSA CC398 originated as MSSA in humans. The jump of CC398 from humans to livestock was accompanied by the loss of phage-carried human virulence genes, which likely attenuated its zoonotic potential, but it was also accompanied by the acquisition of tetracycline and methicillin resistance. Our findings exemplify a bidirectional zoonotic exchange and underscore the potential public health risks of widespread antibiotic use in food animal production. |
| format |
article |
| author |
Lance B. Price Marc Stegger Henrik Hasman Maliha Aziz Jesper Larsen Paal Skytt Andersen Talima Pearson Andrew E. Waters Jeffrey T. Foster James Schupp John Gillece Elizabeth Driebe Cindy M. Liu Burkhard Springer Irena Zdovc Antonio Battisti Alessia Franco Jacek Żmudzki Stefan Schwarz Patrick Butaye Eric Jouy Constanca Pomba M. Concepción Porrero Raymond Ruimy Tara C. Smith D. Ashley Robinson J. Scott Weese Carmen Sofia Arriola Fangyou Yu Frederic Laurent Paul Keim Robert Skov Frank M. Aarestrup |
| author_facet |
Lance B. Price Marc Stegger Henrik Hasman Maliha Aziz Jesper Larsen Paal Skytt Andersen Talima Pearson Andrew E. Waters Jeffrey T. Foster James Schupp John Gillece Elizabeth Driebe Cindy M. Liu Burkhard Springer Irena Zdovc Antonio Battisti Alessia Franco Jacek Żmudzki Stefan Schwarz Patrick Butaye Eric Jouy Constanca Pomba M. Concepción Porrero Raymond Ruimy Tara C. Smith D. Ashley Robinson J. Scott Weese Carmen Sofia Arriola Fangyou Yu Frederic Laurent Paul Keim Robert Skov Frank M. Aarestrup |
| author_sort |
Lance B. Price |
| title |
<named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock |
| title_short |
<named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock |
| title_full |
<named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock |
| title_fullStr |
<named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock |
| title_full_unstemmed |
<named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock |
| title_sort |
<named-content content-type="genus-species">staphylococcus aureus</named-content> cc398: host adaptation and emergence of methicillin resistance in livestock |
| publisher |
American Society for Microbiology |
| publishDate |
2012 |
| url |
https://doaj.org/article/b9fabdb17e9740f3b86c452ad4ee246a |
| work_keys_str_mv |
AT lancebprice namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT marcstegger namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT henrikhasman namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT malihaaziz namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT jesperlarsen namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT paalskyttandersen namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT talimapearson namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT andrewewaters namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT jeffreytfoster namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT jamesschupp namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT johngillece namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT elizabethdriebe namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT cindymliu namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT burkhardspringer namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT irenazdovc namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT antoniobattisti namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT alessiafranco namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT jacekzmudzki namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT stefanschwarz namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT patrickbutaye namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT ericjouy namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT constancapomba namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT mconcepcionporrero namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT raymondruimy namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT taracsmith namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT dashleyrobinson namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT jscottweese namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT carmensofiaarriola namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT fangyouyu namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT fredericlaurent namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT paulkeim namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT robertskov namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock AT frankmaarestrup namedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398hostadaptationandemergenceofmethicillinresistanceinlivestock |
| _version_ |
1718427790392426496 |