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

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Autores principales: van Hal, Sebastiaan J., Steinig, Eike J., Andersson, Patiyan, Holden, Matthew T. G., Harris, Simon R., Nimmo, Graeme R., Williamson, Deborah A., Heffernan, Helen, Ritchie, S. R., Kearns, Angela M., Ellington, Matthew J., Dickson, Elizabeth, de Lencastre, Herminia, Coombs, Geoffrey W., Bentley, Stephen D., Parkhill, Julian, Holt, Deborah C., Giffard, Phillip M., Tong, Steven Y. C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6047344/
https://www.ncbi.nlm.nih.gov/pubmed/30038600
http://dx.doi.org/10.3389/fmicb.2018.01453
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author van Hal, Sebastiaan J.
Steinig, Eike J.
Andersson, Patiyan
Holden, Matthew T. G.
Harris, Simon R.
Nimmo, Graeme R.
Williamson, Deborah A.
Heffernan, Helen
Ritchie, S. R.
Kearns, Angela M.
Ellington, Matthew J.
Dickson, Elizabeth
de Lencastre, Herminia
Coombs, Geoffrey W.
Bentley, Stephen D.
Parkhill, Julian
Holt, Deborah C.
Giffard, Phillip M.
Tong, Steven Y. C.
author_facet van Hal, Sebastiaan J.
Steinig, Eike J.
Andersson, Patiyan
Holden, Matthew T. G.
Harris, Simon R.
Nimmo, Graeme R.
Williamson, Deborah A.
Heffernan, Helen
Ritchie, S. R.
Kearns, Angela M.
Ellington, Matthew J.
Dickson, Elizabeth
de Lencastre, Herminia
Coombs, Geoffrey W.
Bentley, Stephen D.
Parkhill, Julian
Holt, Deborah C.
Giffard, Phillip M.
Tong, Steven Y. C.
author_sort van Hal, Sebastiaan J.
collection PubMed
description 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.
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spelling pubmed-60473442018-07-23 Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia van Hal, Sebastiaan J. Steinig, Eike J. Andersson, Patiyan Holden, Matthew T. G. Harris, Simon R. Nimmo, Graeme R. Williamson, Deborah A. Heffernan, Helen Ritchie, S. R. Kearns, Angela M. Ellington, Matthew J. Dickson, Elizabeth de Lencastre, Herminia Coombs, Geoffrey W. Bentley, Stephen D. Parkhill, Julian Holt, Deborah C. Giffard, Phillip M. Tong, Steven Y. C. Front Microbiol Microbiology 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. Frontiers Media S.A. 2018-07-09 /pmc/articles/PMC6047344/ /pubmed/30038600 http://dx.doi.org/10.3389/fmicb.2018.01453 Text en Copyright © 2018 van Hal, Steinig, Andersson, Holden, Harris, Nimmo, Williamson, Heffernan, Ritchie, Kearns, Ellington, Dickson, de Lencastre, Coombs, Bentley, Parkhill, Holt, Giffard and Tong. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
van Hal, Sebastiaan J.
Steinig, Eike J.
Andersson, Patiyan
Holden, Matthew T. G.
Harris, Simon R.
Nimmo, Graeme R.
Williamson, Deborah A.
Heffernan, Helen
Ritchie, S. R.
Kearns, Angela M.
Ellington, Matthew J.
Dickson, Elizabeth
de Lencastre, Herminia
Coombs, Geoffrey W.
Bentley, Stephen D.
Parkhill, Julian
Holt, Deborah C.
Giffard, Phillip M.
Tong, Steven Y. C.
Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia
title Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia
title_full Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia
title_fullStr Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia
title_full_unstemmed Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia
title_short Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia
title_sort global scale dissemination of st93: a divergent staphylococcus aureus epidemic lineage that has recently emerged from remote northern australia
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6047344/
https://www.ncbi.nlm.nih.gov/pubmed/30038600
http://dx.doi.org/10.3389/fmicb.2018.01453
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