Molecular Characterization of Chimeric Staphylococcus aureus Strains from Waterfowl

Author:

Monecke Stefan123ORCID,Braun Sascha D.12,Collatz Maximillian12ORCID,Diezel Celia12,Müller Elke12,Reinicke Martin12,Cabal Rosel Adriana4ORCID,Feßler Andrea T.56,Hanke Dennis56,Loncaric Igor7ORCID,Schwarz Stefan56ORCID,Cortez de Jäckel Sonia8,Ruppitsch Werner4ORCID,Gavier-Widén Dolores910,Hotzel Helmut11,Ehricht Ralf1212ORCID

Affiliation:

1. Leibniz Institute of Photonic Technology (IPHT), Leibniz Center for Photonics in Infection Research (LPI), 07745 Jena, Germany

2. InfectoGnostics Research Campus, 07743 Jena, Germany

3. Institute for Medical Microbiology and Virology, Dresden University Hospital, 01307 Dresden, Germany

4. Austrian Agency for Health and Food Safety, Institute for Medical Microbiology and Hygiene, 1220 Vienna, Austria

5. Institute of Microbiology and Epizootics, Centre for Infection, Medicine School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany

6. Veterinary Centre for Resistance Research (TZR), School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany

7. Institute of Microbiology, University of Veterinary Medicine, 1210 Vienna, Austria

8. Poultry Clinics and Laboratory Pöppel, 33129 Delbrück, Germany

9. Department of Pathology and Wildlife Disease, National Veterinary Institute (SVA), 75189 Uppsala, Sweden

10. Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences (SLU), 75007 Uppsala, Sweden

11. Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut (Federal Research Institute for Animal Health), 07743 Jena, Germany

12. Institute of Physical Chemistry, Friedrich-Schiller University, 07743 Jena, Germany

Abstract

Staphylococcus aureus 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 S. aureus 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 cna; some also showed a different capsule type and a deviant spa type. Thus, they were subjected to whole-genome sequencing. This revealed multiple insertions of large regions of DNA from other S. aureus 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 oriC; 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 mecA/mecC genes. These findings highlight the role of horizontal gene transfer in the evolution of S. aureus facilitated by SCC elements, by phages, and by a yet undescribed mechanism for large-scale exchange of core genomic DNA.

Funder

German Federal Ministry of Education and Research

Publisher

MDPI AG

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