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Population Genetic Structure of the Staphylococcus intermedius Group: Insights into agr Diversification and the Emergence of Methicillin-Resistant Strains ^,

Centre for Infectious Diseases, Royal (Dick) School of Veterinary Studies, The Chancellor's Building, New Royal Infirmary, University of Edinburgh, Edinburgh EH16 4SB, Scotland, United Kingdom,¹ Centre for Preventive Medicine, Animal Health Trust, Newmarket, Suffolk CB8 7UU,United Kingdom,² Department of Veterinary Pathobiology, Faculty of Life Science, University of Copenhagen, Frederiksberg C, Denmark,³ Dermatology Unit, Division of Veterinary Clinical Sciences, Royal (Dick) School of Veterinary Studies, Easter Bush Veterinary Centre, University of Edinburgh, Roslin, Midlothian, EH25 9RG, Scotland, United Kingdom⁴

Received 20 July 2007/ Accepted 13 September 2007

The population genetic structure of the animal pathogen Staphylococcus intermedius is poorly understood. We carried out a multilocus sequence phylogenetic analysis of isolates from broad host and geographic origins to investigate inter- and intraspecies diversity. We found that isolates phenotypically identified as S. intermedius are differentiated into three closely related species, S. intermedius, Staphylococcus pseudintermedius, and Staphylococcus delphini. S. pseudintermedius, not S. intermedius, is the common cause of canine pyoderma and occasionally causes zoonotic infections of humans. Over 60 extant STs were identified among the S. pseudintermedius isolates examined, including several that were distributed on different continents. As the agr quorum-sensing system of staphylococci is thought to have evolved along lines of speciation within the genus, we examined the allelic variation of agrD, which encodes the autoinducing peptide (AIP). Four AIP variants were encoded by S. pseudintermedius isolates, and identical AIP variants were shared among the three species, suggesting that a common quorum-sensing capacity has been conserved in spite of species differentiation in largely distinct ecological niches. A lack of clonal association of agr alleles suggests that assortive recombination may have contributed to the distribution of agr diversity. Finally, we discovered that the recent emergence of methicillin-resistant strains was due to multiple acquisitions of the mecA gene by different S. pseudintermedius clones found on different continents. Taken together, these data have resolved the population genetic structure of the S. intermedius group, resulting in new insights into its ancient and recent evolution.

Published ahead of print on 28 September 2007.

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