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      Diversity of Staphylococcus aureus Isolates in European Wildlife

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          Abstract

          Staphylococcus aureus is a well-known colonizer and cause of infection among animals and it has been described from numerous domestic and wild animal species. The aim of the present study was to investigate the molecular epidemiology of S. aureus in a convenience sample of European wildlife and to review what previously has been observed in the subject field. 124 S. aureus isolates were collected from wildlife in Germany, Austria and Sweden; they were characterized by DNA microarray hybridization and, for isolates with novel hybridization patterns, by multilocus sequence typing (MLST). The isolates were assigned to 29 clonal complexes and singleton sequence types (CC1, CC5, CC6, CC7, CC8, CC9, CC12, CC15, CC22, CC25, CC30, CC49, CC59, CC88, CC97, CC130, CC133, CC398, ST425, CC599, CC692, CC707, ST890, CC1956, ST2425, CC2671, ST2691, CC2767 and ST2963), some of which (ST2425, ST2691, ST2963) were not described previously. Resistance rates in wildlife strains were rather low and mecA-MRSA isolates were rare ( n = 6). mecC-MRSA ( n = 8) were identified from a fox, a fallow deer, hares and hedgehogs. The common cattle-associated lineages CC479 and CC705 were not detected in wildlife in the present study while, in contrast, a third common cattle lineage, CC97, was found to be common among cervids. No Staphylococcus argenteus or Staphylococcus schweitzeri-like isolates were found. Systematic studies are required to monitor the possible transmission of human- and livestock-associated S. aureus/MRSA to wildlife and vice versa as well as the possible transmission, by unprotected contact to animals. The prevalence of S. aureus/MRSA in wildlife as well as its population structures in different wildlife host species warrants further investigation.

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          A Field Guide to Pandemic, Epidemic and Sporadic Clones of Methicillin-Resistant Staphylococcus aureus

          In recent years, methicillin-resistant Staphylococcus aureus (MRSA) have become a truly global challenge. In addition to the long-known healthcare-associated clones, novel strains have also emerged outside of the hospital settings, in the community as well as in livestock. The emergence and spread of virulent clones expressing Panton-Valentine leukocidin (PVL) is an additional cause for concern. In order to provide an overview of pandemic, epidemic and sporadic strains, more than 3,000 clinical and veterinary isolates of MRSA mainly from Germany, the United Kingdom, Ireland, France, Malta, Abu Dhabi, Hong Kong, Australia, Trinidad & Tobago as well as some reference strains from the United States have been genotyped by DNA microarray analysis. This technique allowed the assignment of the MRSA isolates to 34 distinct lineages which can be clearly defined based on non-mobile genes. The results were in accordance with data from multilocus sequence typing. More than 100 different strains were distinguished based on affiliation to these lineages, SCCmec type and the presence or absence of PVL. These strains are described here mainly with regard to clinically relevant antimicrobial resistance- and virulence-associated markers, but also in relation to epidemiology and geographic distribution. The findings of the study show a high level of biodiversity among MRSA, especially among strains harbouring SCCmec IV and V elements. The data also indicate a high rate of genetic recombination in MRSA involving SCC elements, bacteriophages or other mobile genetic elements and large-scale chromosomal replacements.
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            Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus.

            The impact of globalization on the emergence and spread of pathogens is an important veterinary and public health issue. Staphylococcus aureus is a notorious human pathogen associated with serious nosocomial and community-acquired infections. In addition, S. aureus is a major cause of animal diseases including skeletal infections of poultry, which are a large economic burden on the global broiler chicken industry. Here, we provide evidence that the majority of S. aureus isolates from broiler chickens are the descendants of a single human-to-poultry host jump that occurred approximately 38 years ago (range, 30 to 63 years ago) by a subtype of the worldwide human ST5 clonal lineage unique to Poland. In contrast to human subtypes of the ST5 radiation, which demonstrate strong geographic clustering, the poultry ST5 clade was distributed in different continents, consistent with wide dissemination via the global poultry industry distribution network. The poultry ST5 clade has undergone genetic diversification from its human progenitor strain by acquisition of novel mobile genetic elements from an avian-specific accessory gene pool, and by the inactivation of several proteins important for human disease pathogenesis. These genetic events have resulted in enhanced resistance to killing by chicken heterophils, reflecting avian host-adaptive evolution. Taken together, we have determined the evolutionary history of a major new animal pathogen that has undergone rapid avian host adaptation and intercontinental dissemination. These data provide a new paradigm for the impact of human activities on the emergence of animal pathogens.
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              Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA(LGA251).

              The recent finding of a new mecA homologue, mecA(LGA251) , with only 70% nucleotide homology to the conventional mecA gene has brought the routine testing for mecA as a confirmatory test for methicillin-resistant Staphylococcus aureus (MRSA) into question. A multiplex PCR was designed to differentiate mecA(LGA251) from the known mecA together with detection of lukF-PV and the spa gene fragments, enabling direct spa typing by sequencing of the PCR amplicons. The PCR analysis and subsequent spa typing were validated on a large collection (n=185) of contemporary MRSA and methicillin-sensitive S. aureus isolates, including 127 isolates carrying mecA(LGA251) . The mecA(LGA251) gene was situated in staphylococcal cassette chromosome mec type XI elements, and sequence variation within a 631-bp fragment of mecA(LGA251) in 79 isolates indicated a very conserved gene sequence. Following a successful validation, the multiplex PCR strategy was implemented in the routine testing of MRSA for national surveillance. Over a 2-month period, among 203 samples tested, 12 new MRSA cases caused by isolates carrying mecA(LGA251) were identified, emphasizing the clinical importance of testing for these new MRSA isolates. © 2011 STATENS SERUM INSTITUT. Clinical Microbiology and Infection © 2011 European Society of Clinical Microbiology and Infectious Diseases.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                16 December 2016
                2016
                : 11
                : 12
                : e0168433
                Affiliations
                [1 ]Institute for Medical Microbiology and Hygiene (IMMH), Technical University of Dresden, Dresden, Germany
                [2 ]Alere Technologies GmbH, Jena, Germany
                [3 ]InfectoGnostics Research Campus, Jena, Germany
                [4 ]Department of Pathology and Wildlife Disease, National Veterinary Institute (SVA), Uppsala, Sweden
                [5 ]Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden
                [6 ]Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Bacterial Infections and Zoonoses, Jena, Germany
                [7 ]Chemisches und Veterinäruntersuchungsamt Westfalen, Standort Arnsberg, Arnsberg, Germany
                [8 ]Institute of Microbiology and Epizootics, Veterinary Faculty, Freie Universität Berlin, Berlin, Germany
                [9 ]Microbiology Research Unit, Dublin Dental University Hospital, University of Dublin, Trinity College Dublin, Dublin, Ireland
                [10 ]Institute of Microbiology, University of Veterinary Medicine, Vienna, Austria
                Rockefeller University, UNITED STATES
                Author notes

                Competing Interests: R. Ehricht, E. Müller, A. Reissig and S. Monecke are employees of Alere Technologies, the company that manufactures the microarrays used for this study. The arrays used herein are (or will be developed to be) a marketed product. This does not alter our adherence to PLOS ONE policies on sharing data and materials

                • Conceptualization: SM RE DGW.

                • Data curation: SM DGW RE IL MP HH.

                • Investigation: EM AR ARL AL BW.

                • Project administration: SM RE.

                • Resources: DGW HH MP SG BW IL.

                • Writing – original draft: SM RE.

                • Writing – review & editing: SM RE ACS DCC.

                Article
                PONE-D-16-25247
                10.1371/journal.pone.0168433
                5161505
                27992523
                a7a80673-de8b-4eeb-a3ac-47a99d1ccbfe
                © 2016 Monecke et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 23 June 2016
                : 1 December 2016
                Page count
                Figures: 0, Tables: 3, Pages: 27
                Funding
                Funded by: EU 7thFrame work Program for Research and Technological Development
                Award ID: 222633
                Award Recipient :
                Funded by: Rodent associated pathogens
                Award ID: 01KI1018
                Award Recipient :
                Funded by: Rodent associated pathogens
                Award ID: 01KI1018
                Award Recipient :
                Funded by: EU 7th Framework Program for Research and Technological Development
                Award ID: 111633
                Award Recipient :
                Funded by: German Research Foundation, DFG
                Award ID: GU 1283/3-1
                Award Recipient :
                A part of the work (by D. Gavier-Widén and partially by R. Ehricht) was founded by the EU (Wildtech project; EU 7th Framework Program for Research and Technological Development, grant agreement no. 222633), another (by B. Walter and S. Guenther) by the Network “Rodent associated pathogens” (NaÜPa-Net Grant 01KI1018). S. Guenther was funded by a Grant of the German Research Foundation (Grant GU 1283/3-1). For the other authors, there was no external funding, and their institutions covered the costs of experiments performed in the respective units and granted the time needed to perform this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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