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Front Microbiol. 2018 Jul 9;9:1453. doi: 10.3389/fmicb.2018.01453. eCollection 2018.

Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia.

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Department of Microbiology and Infectious Diseases, Royal Prince Alfred Hospital, Sydney, NSW, Australia.
Global and Tropical Health Division, Menzies School of Health Research, Darwin, NT, Australia.
Australian Institute of Tropical Health and Medicine, Townsville, QLD, Australia.
School of Medicine, University of St. Andrews, Fife, United Kingdom.
Pathogen Genomics, Wellcome Trust Sanger Institute, Cambridge, United Kingdom.
Pathology Queensland Central Laboratory and Griffith University School of Medicine, Queensland Health, Brisbane, QLD, Australia.
Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.
Institute of Environmental Science and Research, Porirua, New Zealand.
School of Medical Sciences, University of Auckland, Auckland, New Zealand.
Antimicrobial Resistance and Healthcare Associated Infections Reference Unit, National Infection Service, Public Health England, London, United Kingdom.
National Infection Service, Public Health England, Addenbrooke's Hospital, Cambridge, United Kingdom.
Scottish MRSA Reference Service, Scottish Microbiology Reference Laboratories, Glasgow Royal Infirmary, Glasgow, United Kingdom.
Laboratory of Molecular Genetics, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, Portugal.
Laboratory of Microbiology and Infectious Diseases, The Rockefeller University, New York, NY, United States.
School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA, Australia.
Department of Microbiology, Fiona Stanley Hospital, Perth, WA, Australia.
Victorian Infectious Disease Service, The Royal Melbourne Hospital, and The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.


Background: In Australia, community-associated methicillin-resistant Staphylococcus aureus (MRSA) lineage sequence type (ST) 93 has rapidly risen to dominance since being described in the early 1990s. We examined 459 ST93 genome sequences from Australia, New Zealand, Samoa, and Europe to investigate the evolutionary history of ST93, its emergence in Australia and subsequent spread overseas. Results: Comparisons with other S. aureus genomes indicate that ST93 is an early diverging and recombinant lineage, comprising of segments from the ST59/ST121 lineage and from a divergent but currently unsampled Staphylococcal population. However, within extant ST93 strains limited genetic diversity was apparent with the most recent common ancestor dated to 1977 (95% highest posterior density 1973-1981). An epidemic ST93 population arose from a methicillin-susceptible progenitor in remote Northern Australia, which has a proportionally large Indigenous population, with documented overcrowded housing and a high burden of skin infection. Methicillin-resistance was acquired three times in these regions, with a clade harboring a staphylococcal cassette chromosome mec (SCCmec) IVa expanding and spreading to Australia's east coast by 2000. We observed sporadic and non-sustained introductions of ST93-MRSA-IVa to the United Kingdom. In contrast, in New Zealand, ST93-MRSA-IVa was sustainably transmitted with clonal expansion within the Pacific Islander population, who experience similar disadvantages as Australian Indigenous populations. Conclusion: ST93 has a highly recombinant genome including portions derived from an early diverging S. aureus population. Our findings highlight the need to understand host population factors in the emergence and spread of antimicrobial resistant community pathogens.


Aboriginal; Indigenous; MRSA; ST93; Staphylococcus aureus; community-associated; evolution

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