Emergence of the Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and <italic toggle="yes">speG</italic>-mediated Adaptations for Survival on Skin

ABSTRACT The arginine catabolic mobile element (ACME) is the largest genomic region distinguishing epidemic USA300 strains of methicillin-resistant Staphylococcus aureus (MRSA) from other S. aureus strains. However, the functional relevance of ACME to infection and disease has remained unclear. Usin...

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Autores principales:	Paul J. Planet, Samuel J. LaRussa, Ali Dana, Hannah Smith, Amy Xu, Chanelle Ryan, Anne-Catrin Uhlemann, Sam Boundy, Julia Goldberg, Apurva Narechania, Ritwij Kulkarni, Adam J. Ratner, Joan A. Geoghegan, Sergios-Orestis Kolokotronis, Alice Prince
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/23678e48e8fd4f5397c09784e28a48a2
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spelling	oai:doaj.org-article:23678e48e8fd4f5397c09784e28a48a22021-11-15T15:42:31ZEmergence of the Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and <italic toggle="yes">speG</italic>-mediated Adaptations for Survival on Skin10.1128/mBio.00889-132150-7511https://doaj.org/article/23678e48e8fd4f5397c09784e28a48a22013-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00889-13https://doaj.org/toc/2150-7511ABSTRACT The arginine catabolic mobile element (ACME) is the largest genomic region distinguishing epidemic USA300 strains of methicillin-resistant Staphylococcus aureus (MRSA) from other S. aureus strains. However, the functional relevance of ACME to infection and disease has remained unclear. Using phylogenetic analysis, we have shown that the modular segments of ACME were assembled into a single genetic locus in Staphylococcus epidermidis and then horizontally transferred to the common ancestor of USA300 strains in an extremely recent event. Acquisition of one ACME gene, speG, allowed USA300 strains to withstand levels of polyamines (e.g., spermidine) produced in skin that are toxic to other closely related S. aureus strains. speG-mediated polyamine tolerance also enhanced biofilm formation, adherence to fibrinogen/fibronectin, and resistance to antibiotic and keratinocyte-mediated killing. We suggest that these properties gave USA300 a major selective advantage during skin infection and colonization, contributing to the extraordinary evolutionary success of this clone. IMPORTANCE Over the past 15 years, methicillin-resistant Staphylococcus aureus (MRSA) has become a major public health problem. It is likely that adaptations in specific MRSA lineages (e.g., USA300) drove the spread of MRSA across the United States and allowed it to replace other, less-virulent S. aureus strains. We suggest that one major factor in the evolutionary success of MRSA may have been the acquisition of a gene (speG) that allows S. aureus to evade the toxicity of polyamines (e.g., spermidine and spermine) that are produced in human skin. Polyamine tolerance likely gave MRSA multiple fitness advantages, including the formation of more-robust biofilms, increased adherence to host tissues, and resistance to antibiotics and killing by human skin cells.Paul J. PlanetSamuel J. LaRussaAli DanaHannah SmithAmy XuChanelle RyanAnne-Catrin UhlemannSam BoundyJulia GoldbergApurva NarechaniaRitwij KulkarniAdam J. RatnerJoan A. GeogheganSergios-Orestis KolokotronisAlice PrinceAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 6 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Paul J. Planet Samuel J. LaRussa Ali Dana Hannah Smith Amy Xu Chanelle Ryan Anne-Catrin Uhlemann Sam Boundy Julia Goldberg Apurva Narechania Ritwij Kulkarni Adam J. Ratner Joan A. Geoghegan Sergios-Orestis Kolokotronis Alice Prince Emergence of the Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and <italic toggle="yes">speG</italic>-mediated Adaptations for Survival on Skin
description	ABSTRACT The arginine catabolic mobile element (ACME) is the largest genomic region distinguishing epidemic USA300 strains of methicillin-resistant Staphylococcus aureus (MRSA) from other S. aureus strains. However, the functional relevance of ACME to infection and disease has remained unclear. Using phylogenetic analysis, we have shown that the modular segments of ACME were assembled into a single genetic locus in Staphylococcus epidermidis and then horizontally transferred to the common ancestor of USA300 strains in an extremely recent event. Acquisition of one ACME gene, speG, allowed USA300 strains to withstand levels of polyamines (e.g., spermidine) produced in skin that are toxic to other closely related S. aureus strains. speG-mediated polyamine tolerance also enhanced biofilm formation, adherence to fibrinogen/fibronectin, and resistance to antibiotic and keratinocyte-mediated killing. We suggest that these properties gave USA300 a major selective advantage during skin infection and colonization, contributing to the extraordinary evolutionary success of this clone. IMPORTANCE Over the past 15 years, methicillin-resistant Staphylococcus aureus (MRSA) has become a major public health problem. It is likely that adaptations in specific MRSA lineages (e.g., USA300) drove the spread of MRSA across the United States and allowed it to replace other, less-virulent S. aureus strains. We suggest that one major factor in the evolutionary success of MRSA may have been the acquisition of a gene (speG) that allows S. aureus to evade the toxicity of polyamines (e.g., spermidine and spermine) that are produced in human skin. Polyamine tolerance likely gave MRSA multiple fitness advantages, including the formation of more-robust biofilms, increased adherence to host tissues, and resistance to antibiotics and killing by human skin cells.
format	article
author	Paul J. Planet Samuel J. LaRussa Ali Dana Hannah Smith Amy Xu Chanelle Ryan Anne-Catrin Uhlemann Sam Boundy Julia Goldberg Apurva Narechania Ritwij Kulkarni Adam J. Ratner Joan A. Geoghegan Sergios-Orestis Kolokotronis Alice Prince
author_facet	Paul J. Planet Samuel J. LaRussa Ali Dana Hannah Smith Amy Xu Chanelle Ryan Anne-Catrin Uhlemann Sam Boundy Julia Goldberg Apurva Narechania Ritwij Kulkarni Adam J. Ratner Joan A. Geoghegan Sergios-Orestis Kolokotronis Alice Prince
author_sort	Paul J. Planet
title	Emergence of the Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and <italic toggle="yes">speG</italic>-mediated Adaptations for Survival on Skin
title_short	Emergence of the Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and <italic toggle="yes">speG</italic>-mediated Adaptations for Survival on Skin
title_full	Emergence of the Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and <italic toggle="yes">speG</italic>-mediated Adaptations for Survival on Skin
title_fullStr	Emergence of the Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and <italic toggle="yes">speG</italic>-mediated Adaptations for Survival on Skin
title_full_unstemmed	Emergence of the Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and <italic toggle="yes">speG</italic>-mediated Adaptations for Survival on Skin
title_sort	emergence of the epidemic methicillin-resistant <named-content content-type="genus-species">staphylococcus aureus</named-content> strain usa300 coincides with horizontal transfer of the arginine catabolic mobile element and <italic toggle="yes">speg</italic>-mediated adaptations for survival on skin
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/23678e48e8fd4f5397c09784e28a48a2
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