Origin, evolution, and global transmission of community-acquired  Staphylococcus aureus  ST8

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Significance

USA300 is a hypervirulent, community-acquired, multidrug-resistant Staphylococcus aureus clone that started to spread in the United States around 17 years ago. Many studies detected it also in South America, Europe, and the Asia-Pacific region. In this study, we show that USA300 is also circulating in sub-Saharan Africa. Locating the temporal and spatial origin of clonal lineages is important with respect to epidemiology and molecular evolution of pathogens. We show that USA300 evolved from a less virulent and less resistant ancestor circulating in Central Europe around 160 years ago. Constant surveillance of pathogen transmission routes is vital to prevent and control potential outbreaks. Whole genome sequencing proved to be a useful tool for epidemiological surveillance.

Abstract

USA300 is a pandemic clonal lineage of hypervirulent, community-acquired, methicillin-resistant Staphylococcus aureus (CA-MRSA) with specific molecular characteristics. Despite its high clinical relevance, the evolutionary origin of USA300 remained unclear. We used comparative genomics of 224 temporal and spatial diverse S. aureus isolates of multilocus sequence type (ST) 8 to reconstruct the molecular evolution and global dissemination of ST8, including USA300. Analyses of core SNP diversity and accessory genome variations showed that the ancestor of all ST8 S. aureus most likely emerged in Central Europe in the mid-19th century. From here, ST8 was exported to North America in the early 20th century and progressively acquired the USA300 characteristics Panton–Valentine leukocidin (PVL), SCC mec IVa, the arginine catabolic mobile element (ACME), and a specific mutation in capsular polysaccharide gene cap5E. Although the PVL-encoding phage ϕSa2USA was introduced into the ST8 background only once, various SCC mec types were introduced to ST8 at different times and places. Starting from North America, USA300 spread globally, including Africa. African USA300 isolates have aberrant spa-types (t112, t121) and form a monophyletic group within the clade of North American USA300. Large parts of ST8 methicillin-susceptible S. aureus (MSSA) isolated in Africa represent a symplesiomorphic group of ST8 (i.e., a group representing the characteristics of the ancestor), which are rarely found in other world regions. Isolates previously discussed as USA300 ancestors, including USA500 and a “historic” CA-MRSA from Western Australia, were shown to be only distantly related to recent USA300 clones.

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Most cited references 56

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Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database.

Linda K. McDougal, Christine Steward, George Killgore … (2003)

Oxacillin-resistant Staphylococcus aureus (ORSA) is a virulent pathogen responsible for both health care-associated and community onset disease. We used SmaI-digested genomic DNA separated by pulsed-field gel electrophoresis (PFGE) to characterize 957 S. aureus isolates and establish a database of PFGE patterns. In addition to PFGE patterns of U.S. strains, the database contains patterns of representative epidemic-type strains from the United Kingdom, Canada, and Australia; previously described ORSA clonal-type isolates; 13 vancomycin-intermediate S. aureus (VISA) isolates, and two high-level vancomycin-resistant, vanA-positive strains (VRSA). Among the isolates from the United States, we identified eight lineages, designated as pulsed-field types (PFTs) USA100 through USA800, seven of which included both ORSA and oxacillin-susceptible S. aureus isolates. With the exception of the PFT pairs USA100 and USA800, and USA300 and USA500, each of the PFTs had a unique multilocus sequence type and spa type motif. The USA100 PFT, previously designated as the New York/Tokyo clone, was the most common PFT in the database, representing 44% of the ORSA isolates. USA100 isolates were typically multiresistant and included all but one of the U.S. VISA strains and both VRSA isolates. Multiresistant ORSA isolates from the USA200, -500, and -600 PFTs have PFGE patterns similar to those of previously described epidemic strains from Europe and Australia. The USA300 and -400 PFTs contained community isolates resistant only to beta-lactam drugs and erythromycin. Noticeably absent from the U.S. database were isolates with the previously described Brazilian and EMRSA15 PFGE patterns. These data suggest that there are a limited number of ORSA genotypes present in the United States.

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Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak.

Claudio Köser, Matthew T.G. Holden, Matthew Ellington … (2012)

Isolates of methicillin-resistant Staphylococcus aureus (MRSA) belonging to a single lineage are often indistinguishable by means of current typing techniques. Whole-genome sequencing may provide improved resolution to define transmission pathways and characterize outbreaks. We investigated a putative MRSA outbreak in a neonatal intensive care unit. By using rapid high-throughput sequencing technology with a clinically relevant turnaround time, we retrospectively sequenced the DNA from seven isolates associated with the outbreak and another seven MRSA isolates associated with carriage of MRSA or bacteremia in the same hospital. We constructed a phylogenetic tree by comparing single-nucleotide polymorphisms (SNPs) in the core genome to a reference genome (an epidemic MRSA clone, EMRSA-15 [sequence type 22]). This revealed a distinct cluster of outbreak isolates and clear separation between these and the nonoutbreak isolates. A previously missed transmission event was detected between two patients with bacteremia who were not part of the outbreak. We created an artificial "resistome" of antibiotic-resistance genes and demonstrated concordance between it and the results of phenotypic susceptibility testing; we also created a "toxome" consisting of toxin genes. One outbreak isolate had a hypermutator phenotype with a higher number of SNPs than the other outbreak isolates, highlighting the difficulty of imposing a simple threshold for the number of SNPs between isolates to decide whether they are part of a recent transmission chain. Whole-genome sequencing can provide clinically relevant data within a time frame that can influence patient care. The need for automated data interpretation and the provision of clinically meaningful reports represent hurdles to clinical implementation. (Funded by the U.K. Clinical Research Collaboration Translational Infection Research Initiative and others.).

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Methicillin-resistant Staphylococcus aureus strain USA300: origin and epidemiology.

Fred Tenover, Richard V Goering (2009)

Methicillin-resistant Staphylococcus aureus (MRSA) PFGE strain type USA300 (multilocus sequence type 8, clonal complex 8, staphylococcal cassette chromosome mec type IV) was first reported in the USA as a cause of skin and soft issue infection among college football players in Pennsylvania and among prisoners in Missouri in 2000. Over the next 5 years, USA300 became the predominant community-associated MRSA strain in the USA. It was the most common PFGE type recovered from skin and soft tissue infections in persons presenting to 11 emergency departments across the USA, and caused outbreaks in Native American populations, children in daycare centres, military recruits, prison inmates and among men who have sex with men. Although predominantly a cause of skin and soft issue infection, USA300 isolates also have been recovered from cases of invasive disease including bacteraemia, endocarditis, severe necrotizing pneumonia and osteomyelitis. Isolates of USA300 usually carry the genes encoding the Panton-Valentine leucocidin and the arginine catabolic mobile element, but rarely carry staphylococcal enterotoxin genes. USA300 isolates are becoming more resistant to antimicrobial agents, including erythromycin, levofloxacin, mupirocin and tetracycline, and have spread to Europe, South America and Australia. The emergence of the MRSA USA300 strain type represents a unique biological success story.

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Author and article information

Journal

Journal ID (nlm-ta): Proc Natl Acad Sci U S A

Journal ID (iso-abbrev): Proc. Natl. Acad. Sci. U.S.A

Journal ID (hwp): pnas

Journal ID (pmc): pnas

Journal ID (publisher-id): PNAS

Title: Proceedings of the National Academy of Sciences of the United States of America

Publisher: National Academy of Sciences

ISSN (Print): 0027-8424

ISSN (Electronic): 1091-6490

Publication date (Print): 5 December 2017

Publication date (Electronic): 20 November 2017

Publication date PMC-release: 20 November 2017

Volume: 114

Issue: 49

Pages: E10596-E10604

Affiliations

[1] ^aInstitute of Hygiene, University Hospital Münster , DE 48149 Münster, Germany;

[2] ^bDepartment of Bacteria, Parasites, and Fungi, Statens Serum Institut , DK 2300 Copenhagen, Denmark;

[3] ^cPathogen Genomics Division, Translational Genomics Research Institute , Flagstaff, AZ 86005;

[4] ^dDepartment of Paraclinical Sciences, The University of the West Indies , St. Augustine, Trinidad and Tobago;

[5] ^eDepartment of Microbiology, Centre de Recherches Médicales de Lambaréné , GA 242 Lambaréné, Gabon;

[6] ^fInstitute of Tropical Medicine, German Center for Infection Research, Eberhard Karls University , DE 72076 Tübingen, Germany;

[7] ^gFaculty of Medicine, University Hospital of Pointe-à-Pitre, University of the French West Indies , 97110 Pointe-à-Pitre, Guadeloupe, France;

[8] ^hUnité Environnement et Santé, Institut Pasteur de Guadeloupe , 97110 Pointe-à-Pitre, Guadeloupe, France;

[9] ⁱSchool of Veterinary and Laboratory Sciences, Murdoch University, Western Australia, Australia, 6150;

[10] ^jPathWest Laboratory Medicine WA, Fiona Stanley Hospital, Western Australia, Australia 6150;

[11] ^kDepartment of Bacteriology, Noguchi Memorial Institute for Medical Research , LG581 Accra, Ghana;

[12] ^lNational Reference Center for Staphylococci, Hospices Civils de Lyon, University of Lyon , FR 69002 Lyon, France;

[13] ^mInstitute for Medical Microbiology and Hygiene, Technical University of Dresden , DE 01307 Dresden, Germany;

[14] ⁿAlere Technologies , DE 07749 Jena, Germany;

[15] ^oInstitute of Medical Microbiology, University Hospital Münster , DE 48149 Münster, Germany;

[16] ^pClinical Microbiology, Medizinisches Versorgungszentrum SYNLAB Leverkusen GmbH , DE 51375 Leverkusen, Germany;

[17] ^qNational Reference Centre for Staphylococci and Enterococci, Wernigerode Branch, Robert-Koch-Institut , DE 38855 Wernigerode, Germany

Author notes

¹To whom correspondence should be addressed. Email: mellmann@ 123456uni-Muenster.de .

Edited by Richard P. Novick, New York University School of Medicine, New York, NY, and approved October 18, 2017 (received for review February 13, 2017)

Author contributions: L.S., M.S., G.P., R.S., F.S., and A.M. designed research; L.S., M.S., P.E.A., A.A., S.B., G.C., B.E., A.R.L., F.L., S.M., B.S., F.V., F.S., and A.M. performed research; L.S., M.S., and A.M. analyzed data; and L.S., M.S., and A.M. wrote the paper.