Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content>
ABSTRACT The importance of livestock as a source of bacterial pathogens with the potential for epidemic spread in human populations is unclear. In recent years, there has been a global increase in community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections of healthy humans...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2013-08-01
|
| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00356-13 |
| _version_ | 1818987338208903168 |
|---|---|
| author | Laura E. Spoor Paul R. McAdam Lucy A. Weinert Andrew Rambaut Henrik Hasman Frank M. Aarestrup Angela M. Kearns Anders R. Larsen Robert L. Skov J. Ross Fitzgerald |
| author_facet | Laura E. Spoor Paul R. McAdam Lucy A. Weinert Andrew Rambaut Henrik Hasman Frank M. Aarestrup Angela M. Kearns Anders R. Larsen Robert L. Skov J. Ross Fitzgerald |
| author_sort | Laura E. Spoor |
| collection | DOAJ |
| description | ABSTRACT The importance of livestock as a source of bacterial pathogens with the potential for epidemic spread in human populations is unclear. In recent years, there has been a global increase in community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections of healthy humans, but an understanding of the different evolutionary origins of CA-MRSA clones and the basis for their recent expansion is lacking. Here, using a high-resolution phylogenetic approach, we report the discovery of two emergent clones of human epidemic CA-MRSA which resulted from independent livestock-to-human host jumps by the major bovine S. aureus complex, CC97. Of note, one of the new clones was isolated from human infections on four continents, demonstrating its global dissemination since the host jump occurred over 40 years ago. The emergence of both human S. aureus clones coincided with the independent acquisition of mobile genetic elements encoding antimicrobial resistance and human-specific mediators of immune evasion, consistent with an important role for these genetic events in the capacity to survive and transmit among human populations. In conclusion, we provide evidence that livestock represent a reservoir for the emergence of new human-pathogenic S. aureus clones with the capacity for pandemic spread. These findings have major public health implications highlighting the importance of surveillance for early identification of emergent clones and improved transmission control measures at the human-livestock interface. IMPORTANCE Animals are the major source of new pathogens affecting humans. However, the potential for pathogenic bacteria that originally were found in animals to switch hosts and become widely established in human populations is not clear. Here, we report the discovery of emergent clones of methicillin-resistant Staphylococcus aureus (MRSA) that originated in livestock and switched to humans, followed by host-adaptive evolution and epidemic spread in global human populations. Our findings demonstrate that livestock can act as a reservoir for the emergence of new human bacterial clones with potential for pandemic spread, highlighting the potential role of surveillance and biosecurity measures in the agricultural setting for preventing the emergence of new human pathogens. |
| first_indexed | 2024-12-20T19:05:06Z |
| format | Article |
| id | doaj.art-e7354c8f5aa84da9b2b11182630efc2c |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-20T19:05:06Z |
| publishDate | 2013-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-e7354c8f5aa84da9b2b11182630efc2c2022-12-21T19:29:18ZengAmerican Society for MicrobiologymBio2150-75112013-08-014410.1128/mBio.00356-13Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content>Laura E. Spoor0Paul R. McAdam1Lucy A. Weinert2Andrew Rambaut3Henrik Hasman4Frank M. Aarestrup5Angela M. Kearns6Anders R. Larsen7Robert L. Skov8J. Ross Fitzgerald9The Roslin Institute and Edinburgh Infectious Diseases, University of Edinburgh, Easter Bush, Midlothian, United KingdomThe Roslin Institute and Edinburgh Infectious Diseases, University of Edinburgh, Easter Bush, Midlothian, United KingdomUniversity of Cambridge, Department of Veterinary Medicine, Cambridge, United KingdomInstitute of Evolutionary Biology, Ashworth Laboratories, University of Edinburgh, Edinburgh, United KingdomNational Food Institute, Technical University of Denmark (DTU), Lyngby, DenmarkNational Food Institute, Technical University of Denmark (DTU), Lyngby, DenmarkMicrobiology Services, Colindale, Health Protection Agency, London, United KingdomDepartment of Antimicrobial Surveillance and Research, Statens Serum Institute, Copenhagen, DenmarkDepartment of Antimicrobial Surveillance and Research, Statens Serum Institute, Copenhagen, DenmarkThe Roslin Institute and Edinburgh Infectious Diseases, University of Edinburgh, Easter Bush, Midlothian, United KingdomABSTRACT The importance of livestock as a source of bacterial pathogens with the potential for epidemic spread in human populations is unclear. In recent years, there has been a global increase in community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections of healthy humans, but an understanding of the different evolutionary origins of CA-MRSA clones and the basis for their recent expansion is lacking. Here, using a high-resolution phylogenetic approach, we report the discovery of two emergent clones of human epidemic CA-MRSA which resulted from independent livestock-to-human host jumps by the major bovine S. aureus complex, CC97. Of note, one of the new clones was isolated from human infections on four continents, demonstrating its global dissemination since the host jump occurred over 40 years ago. The emergence of both human S. aureus clones coincided with the independent acquisition of mobile genetic elements encoding antimicrobial resistance and human-specific mediators of immune evasion, consistent with an important role for these genetic events in the capacity to survive and transmit among human populations. In conclusion, we provide evidence that livestock represent a reservoir for the emergence of new human-pathogenic S. aureus clones with the capacity for pandemic spread. These findings have major public health implications highlighting the importance of surveillance for early identification of emergent clones and improved transmission control measures at the human-livestock interface. IMPORTANCE Animals are the major source of new pathogens affecting humans. However, the potential for pathogenic bacteria that originally were found in animals to switch hosts and become widely established in human populations is not clear. Here, we report the discovery of emergent clones of methicillin-resistant Staphylococcus aureus (MRSA) that originated in livestock and switched to humans, followed by host-adaptive evolution and epidemic spread in global human populations. Our findings demonstrate that livestock can act as a reservoir for the emergence of new human bacterial clones with potential for pandemic spread, highlighting the potential role of surveillance and biosecurity measures in the agricultural setting for preventing the emergence of new human pathogens.https://journals.asm.org/doi/10.1128/mBio.00356-13 |
| spellingShingle | Laura E. Spoor Paul R. McAdam Lucy A. Weinert Andrew Rambaut Henrik Hasman Frank M. Aarestrup Angela M. Kearns Anders R. Larsen Robert L. Skov J. Ross Fitzgerald Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> mBio |
| title | Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_full | Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_fullStr | Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_full_unstemmed | Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_short | Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> |
| title_sort | livestock origin for a human pandemic clone of community associated methicillin resistant named content content type genus species staphylococcus aureus named content |
| url | https://journals.asm.org/doi/10.1128/mBio.00356-13 |
| work_keys_str_mv | AT lauraespoor livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT paulrmcadam livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT lucyaweinert livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT andrewrambaut livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT henrikhasman livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT frankmaarestrup livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT angelamkearns livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT andersrlarsen livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT robertlskov livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent AT jrossfitzgerald livestockoriginforahumanpandemiccloneofcommunityassociatedmethicillinresistantnamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontent |