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Research Article

Staphylococcus aureus CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock

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
Fernando Baquero, Editor
Lance B. Price
Translational Genomics Research Institute (TGen), Pathogen Genomics Division, Flagstaff, Arizona, USAa
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Marc Stegger
Department of Microbiological Surveillance and Research, Statens Serum Institut, Copenhagen, Denmarkb
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Henrik Hasman
National Food Institute, Technical University of Denmark, Lyngby, Denmarkc
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Maliha Aziz
Translational Genomics Research Institute (TGen), Pathogen Genomics Division, Flagstaff, Arizona, USAa
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Jesper Larsen
Department of Microbiological Surveillance and Research, Statens Serum Institut, Copenhagen, Denmarkb
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Paal Skytt Andersen
Department of Microbiological Surveillance and Research, Statens Serum Institut, Copenhagen, Denmarkb
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Talima Pearson
Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USAd
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Andrew E. Waters
Translational Genomics Research Institute (TGen), Pathogen Genomics Division, Flagstaff, Arizona, USAa
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Jeffrey T. Foster
Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USAd
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James Schupp
Translational Genomics Research Institute (TGen), Pathogen Genomics Division, Flagstaff, Arizona, USAa
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John Gillece
Translational Genomics Research Institute (TGen), Pathogen Genomics Division, Flagstaff, Arizona, USAa
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Elizabeth Driebe
Translational Genomics Research Institute (TGen), Pathogen Genomics Division, Flagstaff, Arizona, USAa
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Cindy M. Liu
Translational Genomics Research Institute (TGen), Pathogen Genomics Division, Flagstaff, Arizona, USAa
Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USAd
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Burkhard Springer
Österreichische Agentur für Gesundheit und Ernährungssicherheit GmbH, Bereich Humanmedizin, Institut für Medizinische Mikrobiologie und Hygiene, Graz, Austriae
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Irena Zdovc
Veterinary Faculty, Institute of Microbiology and Parasitology, University of Ljubljana, Ljubljana, Sloveniaf
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Antonio Battisti
Istituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana, Rome, Italyg
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Alessia Franco
Istituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana, Rome, Italyg
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Jacek Żmudzki
Department of Swine Diseases, National Veterinary Research Institute, Pulawy, Polandh
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Stefan Schwarz
Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut, Neustadt-Mariensee, Germanyi
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Patrick Butaye
Department of Pathology, Bacteriology, and Poultry Diseases, Faculty of Veterinary Medicine, University of Ghent, Merelbeke, Belgiumj
Unit of General Bacteriology, Veterinary and Agrochemical Research Centre, Brussels, Belgiumk
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Eric Jouy
Anses, Ploufragan Plouzané Laboratory, Ploufragan, Francel
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Constanca Pomba
Interdisciplinary Centre of Research in Animal Health, Faculty of Veterinary Medicine, Lisbon, Portugalm
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M. Concepción Porrero
Centro de Vigilancia Sanitaria Veterinaria, Universidad Complutense de Madrid, Madrid, Spainn
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Raymond Ruimy
University Paris-Diderot and National Reference Center, Bacterial Resistance in the Commensal Flora, Hôpital Bichat-Claude Bernard, Paris, Franceo
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Tara C. Smith
Center for Emerging Infectious Diseases, University of Iowa, Coralville, Iowa, USAp
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D. Ashley Robinson
Department of Microbiology, University of Mississippi Medical Center, Jackson, Mississippi, USAq
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J. Scott Weese
Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canadar
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Carmen Sofia Arriola
Department of Preventive Veterinary Medicine, San Marcos Major National University, Lima, Perus
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Fangyou Yu
Department of Laboratory Medicine, First Affiliated Hospital of Wenzhou Medical College, Wenzhou, Chinat
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Frederic Laurent
Laboratory of Bacteriology, Hôpital de la Croix Rousse, National Reference Center for Staphylococci, Lyon, Franceu
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Paul Keim
Translational Genomics Research Institute (TGen), Pathogen Genomics Division, Flagstaff, Arizona, USAa
Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USAd
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Robert Skov
Department of Microbiological Surveillance and Research, Statens Serum Institut, Copenhagen, Denmarkb
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Frank M. Aarestrup
National Food Institute, Technical University of Denmark, Lyngby, Denmarkc
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Fernando Baquero
Ramón y Cajal University Hospital
Roles: Editor
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DOI: 10.1128/mBio.00305-11
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This article has a correction. Please see:

  • Staphylococcus aureus CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock
    - January 08, 2013

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.

  • Copyright © 2012 Price 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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Staphylococcus aureus CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock
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
mBio Feb 2012, 3 (1) e00305-11; DOI: 10.1128/mBio.00305-11

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Staphylococcus aureus CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock
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
mBio Feb 2012, 3 (1) e00305-11; DOI: 10.1128/mBio.00305-11
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