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Open AccessArticle

Molecular Epidemiology of Methicillin-Susceptible and Methicillin-Resistant Staphylococcus aureus in Wild, Captive and Laboratory Rats: Effect of Habitat on the Nasal S. aureus Population

1
Department of Immunology, University Medicine Greifswald, 17475 Greifswald, Germany
2
Department of Microbiology and Immunology, Faculty of Pharmacy, Alexandria University, Alexandria 21521, Egypt
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Friedrich-Loeffler-Institute, Federal Research Institute for Animal Health, Institute of Novel and Emerging Infectious Diseases, 17493 Greifswald-Insel Riems, Germany
4
Research and Professional Services, Charles River Laboratories, Wilmington, MA 01887, USA
5
Julius Kühn-Institute, Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Horticulture and Forestry, Vertebrate Research, 48161 Münster, Germany
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Outpatient Clinic, University of Potsdam, 14469 Potsdam, Germany
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Institute of Geoecology, Landscape Ecology & Environmental Systems Analysis, Technische Universität Braunschweig, 38106 Braunschweig, Germany
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von Opel Hessische Zoostiftung, 61476 Kronberg im Taunus, Germany
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Department of Ecology and Diseases of Game, Fish and Bees, University of Veterinary and Pharmaceutical Sciences Brno, 61242 Brno, Czech Republic
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CEITEC—Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences Brno, 61242 Brno, Czech Republic
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Central Core & Research Facility of Laboratory Animals, University Medicine Greifswald, 17475 Greifswald, Germany
12
German Cancer Research Center (DKFZ), Microbiological Diagnostics, 69120 Heidelberg, Germany
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Leibniz Institute of Photonic Technology (IPHT), 07745 Jena, Germany
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Institute for Medical Microbiology and Hygiene, Technical University of Dresden, 01307 Dresden, Germany
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National Reference Centre for Staphylococci and Enterococci, Robert-Koch-Institute, Wernigerode Branch, 38855 Wernigerode, Germany
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Institute of Medical Microbiology, University Hospital Münster, 48149 Münster, Germany
17
Friedrich Loeffler-Institute of Medical Microbiology, University Medicine Greifswald, 17475 Greifswald, Germany
18
German Center for Infection Research (DZIF), Partner Site Hamburg-Lübeck-Borstel-Insel Riems, 17493 Greifswald-Insel Riems, Germany
*
Author to whom correspondence should be addressed.
Current address: Grünenthal GmbH, 52224 Stolberg, Germany
Current address: Office of Animal Resources, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA
Toxins 2020, 12(2), 80; https://doi.org/10.3390/toxins12020080
Received: 20 December 2019 / Revised: 10 January 2020 / Accepted: 20 January 2020 / Published: 24 January 2020
Rats are a reservoir of human- and livestock-associated methicillin-resistant Staphylococcus aureus (MRSA). However, the composition of the natural S. aureus population in wild and laboratory rats is largely unknown. Here, 144 nasal S. aureus isolates from free-living wild rats, captive wild rats and laboratory rats were genotyped and profiled for antibiotic resistances and human-specific virulence genes. The nasal S. aureus carriage rate was higher among wild rats (23.4%) than laboratory rats (12.3%). Free-living wild rats were primarily colonized with isolates of clonal complex (CC) 49 and CC130 and maintained these strains even in husbandry. Moreover, upon livestock contact, CC398 isolates were acquired. In contrast, laboratory rats were colonized with many different S. aureus lineages—many of which are commonly found in humans. Five captive wild rats were colonized with CC398-MRSA. Moreover, a single CC30-MRSA and two CC130-MRSA were detected in free-living or captive wild rats. Rat-derived S. aureus isolates rarely harbored the phage-carried immune evasion gene cluster or superantigen genes, suggesting long-term adaptation to their host. Taken together, our study revealed a natural S. aureus population in wild rats, as well as a colonization pressure on wild and laboratory rats by exposure to livestock- and human-associated S. aureus, respectively.
Keywords: Staphylococcus aureus; rat; clonal complex; host adaptation; livestock; laboratory; coagulation; immune evasion cluster; habitat; epidemiology Staphylococcus aureus; rat; clonal complex; host adaptation; livestock; laboratory; coagulation; immune evasion cluster; habitat; epidemiology
MDPI and ACS Style

Raafat, D.; Mrochen, D.M.; Al’Sholui, F.; Heuser, E.; Ryll, R.; Pritchett-Corning, K.R.; Jacob, J.; Walther, B.; Matuschka, F.-R.; Richter, D.; Westerhüs, U.; Pikula, J.; van den Brandt, J.; Nicklas, W.; Monecke, S.; Strommenger, B.; van Alen, S.; Becker, K.; Ulrich, R.G.; Holtfreter, S. Molecular Epidemiology of Methicillin-Susceptible and Methicillin-Resistant Staphylococcus aureus in Wild, Captive and Laboratory Rats: Effect of Habitat on the Nasal S. aureus Population. Toxins 2020, 12, 80.

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