| Summary: | <i>Staphylococcus aureus</i> is a versatile pathogen that does not only occur in humans but also in various wild and domestic animals, including several avian species. When characterizing <i>S. aureus</i> isolates from waterfowl, isolates were identified as atypical CC133 by DNA microarray analysis. They differed from previously sequenced CC133 strains in the presence of the collagen adhesin gene <i>cna</i>; some also showed a different capsule type and a deviant <i>spa</i> type. Thus, they were subjected to whole-genome sequencing. This revealed multiple insertions of large regions of DNA from other <i>S. aureus</i> lineages into a CC133-derived backbone genome. Three distinct strains were identified based on the size and extent of these inserts. One strain comprised two small inserts of foreign DNA up- and downstream of <i>oriC</i>; one of about 7000 nt or 0.25% originated from CC692 and the other, at ca. 38,000 nt or 1.3% slightly larger one was of CC522 provenance. The second strain carried a larger CC692 insert (nearly 257,000 nt or 10% of the strain’s genome), and its CC522-derived insert was also larger, at about 53,500 nt or 2% of the genome). The third strain carried an identical CC692-derived region (in which the same mutations were observed as in the second strain), but it had a considerably larger CC522-like insertion of about 167,000 nt or 5.9% of the genome. Both isolates of the first, and two out of four isolates of the second strain also harbored a hemolysin-beta-integrating prophage carrying “bird-specific” virulence factors, ornithine cyclodeaminase D0K6J8 and a putative protease D0K6J9. Furthermore, isolates had two different variants of SCC elements that lacked <i>mecA/mecC</i> genes. These findings highlight the role of horizontal gene transfer in the evolution of <i>S. aureus</i> facilitated by SCC elements, by phages, and by a yet undescribed mechanism for large-scale exchange of core genomic DNA.
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