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mBio. Emergence of the Epidemic Methicillin-Resistant Staphylococcus aureus Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and speG-mediated Adaptations for Survival on Skin
[Source: mBio, full page: (LINK). Abstract, edited.]
Emergence of the Epidemic Methicillin-Resistant Staphylococcus aureus Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and speG-mediated Adaptations for Survival on Skin
Paul J. Planet<SUP>a,b</SUP>, Samuel J. LaRussa<SUP>a</SUP>, Ali Dana<SUP>c</SUP>, Hannah Smith<SUP>a</SUP>, Amy Xu<SUP>a</SUP>, Chanelle Ryan<SUP>a</SUP>, Anne-Catrin Uhlemann<SUP>d</SUP>, Sam Boundy<SUP>e</SUP>, Julia Goldberg<SUP>a</SUP>, Apurva Narechania<SUP>b</SUP>, Ritwij Kulkarni<SUP>a</SUP>, Adam J. Ratner<SUP>a</SUP>, Joan A. Geoghegan<SUP>f</SUP>, Sergios-Orestis Kolokotronis<SUP>b,g</SUP>, Alice Prince<SUP>a</SUP>
<SUP></SUP>
Author Affiliations: Division of Pediatric Infectious Diseases, Department of Pediatrics, Columbia University, College of Physicians and Surgeons, New York, New York, USA<SUP>a; </SUP>Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, New York, USA<SUP>b; </SUP>Department of Dermatology, James J. Peters Veterans Affairs Medical Center, Bronx, New York, USA<SUP>c; </SUP>Department of Internal Medicine, Division of Infectious Diseases, Columbia University, College of Physicians and Surgeons, New York, New York, USA<SUP>d; </SUP>Department of Internal Medicine, Division of Infectious Diseases, Virginia Commonwealth University School of Medicine, Richmond, Virginia, USA<SUP>e; </SUP>Department of Microbiology, Moyne Institute of Preventive Medicine, Trinity College, Dublin, Ireland<SUP>f; </SUP>Department of Biological Sciences, Fordham University, Bronx, New York, USA<SUP>g</SUP>
<SUP></SUP>
Address correspondence to Paul J. Planet, pjp23@columbia.edu.
Editor Howard Shuman, University of Chicago
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.
Footnotes
Citation Planet PJ, LaRussa SJ, Dana A, Smith H, Xu A, Ryan C, Uhlemann A-C, Boundy S, Goldberg J, Narechania A, Kulkarni R, Ratner AJ, Geoghegan JA, Kolokotronis S-O, Prince A. 2013. Emergence of the epidemic methicillin-resistant Staphylococcus aureus strain USA300 coincides with horizontal transfer of the arginine catabolic mobile element and speG-mediated adaptations for survival on skin. mBio 4(6):e00889-13. doi:10.1128/mBio.00889-13.
Received 17 October 2013 - Accepted 20 November 2013 - Published 17 December 2013
Copyright ? 2013 Planet et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Emergence of the Epidemic Methicillin-Resistant Staphylococcus aureus Strain USA300 Coincides with Horizontal Transfer of the Arginine Catabolic Mobile Element and speG-mediated Adaptations for Survival on Skin
Paul J. Planet<SUP>a,b</SUP>, Samuel J. LaRussa<SUP>a</SUP>, Ali Dana<SUP>c</SUP>, Hannah Smith<SUP>a</SUP>, Amy Xu<SUP>a</SUP>, Chanelle Ryan<SUP>a</SUP>, Anne-Catrin Uhlemann<SUP>d</SUP>, Sam Boundy<SUP>e</SUP>, Julia Goldberg<SUP>a</SUP>, Apurva Narechania<SUP>b</SUP>, Ritwij Kulkarni<SUP>a</SUP>, Adam J. Ratner<SUP>a</SUP>, Joan A. Geoghegan<SUP>f</SUP>, Sergios-Orestis Kolokotronis<SUP>b,g</SUP>, Alice Prince<SUP>a</SUP>
<SUP></SUP>
Author Affiliations: Division of Pediatric Infectious Diseases, Department of Pediatrics, Columbia University, College of Physicians and Surgeons, New York, New York, USA<SUP>a; </SUP>Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, New York, USA<SUP>b; </SUP>Department of Dermatology, James J. Peters Veterans Affairs Medical Center, Bronx, New York, USA<SUP>c; </SUP>Department of Internal Medicine, Division of Infectious Diseases, Columbia University, College of Physicians and Surgeons, New York, New York, USA<SUP>d; </SUP>Department of Internal Medicine, Division of Infectious Diseases, Virginia Commonwealth University School of Medicine, Richmond, Virginia, USA<SUP>e; </SUP>Department of Microbiology, Moyne Institute of Preventive Medicine, Trinity College, Dublin, Ireland<SUP>f; </SUP>Department of Biological Sciences, Fordham University, Bronx, New York, USA<SUP>g</SUP>
<SUP></SUP>
Address correspondence to Paul J. Planet, pjp23@columbia.edu.
Editor Howard Shuman, University of Chicago
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.
Footnotes
Citation Planet PJ, LaRussa SJ, Dana A, Smith H, Xu A, Ryan C, Uhlemann A-C, Boundy S, Goldberg J, Narechania A, Kulkarni R, Ratner AJ, Geoghegan JA, Kolokotronis S-O, Prince A. 2013. Emergence of the epidemic methicillin-resistant Staphylococcus aureus strain USA300 coincides with horizontal transfer of the arginine catabolic mobile element and speG-mediated adaptations for survival on skin. mBio 4(6):e00889-13. doi:10.1128/mBio.00889-13.
Received 17 October 2013 - Accepted 20 November 2013 - Published 17 December 2013
Copyright ? 2013 Planet et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
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