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Prophage exotoxins enhance colonization fitness in epidemic scarlet fever-causing Streptococcus pyogenes

Author

Listed:
  • Stephan Brouwer

    (The University of Queensland)

  • Timothy C. Barnett

    (The University of Queensland
    University of Western Australia)

  • Diane Ly

    (Illawarra Health and Medical Research Institute
    University of Wollongong)

  • Katherine J. Kasper

    (Western University)

  • David M. P. Oliveira

    (The University of Queensland)

  • Tania Rivera-Hernandez

    (The University of Queensland)

  • Amanda J. Cork

    (The University of Queensland)

  • Liam McIntyre

    (The University of Melbourne)

  • Magnus G. Jespersen

    (The University of Melbourne)

  • Johanna Richter

    (The University of Queensland)

  • Benjamin L. Schulz

    (The University of Queensland)

  • Gordon Dougan

    (The Wellcome Trust Sanger Institute
    University of Cambridge)

  • Victor Nizet

    (University of California San Diego)

  • Kwok-Yung Yuen

    (The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region
    The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region
    The University of Hong Kong-Shenzhen Hospital, Shenzhen, Guangdong Province)

  • Yuanhai You

    (Chinese Centre for Disease Control and Prevention)

  • John K. McCormick

    (Western University
    Lawson Health Research Institute)

  • Martina L. Sanderson-Smith

    (Illawarra Health and Medical Research Institute
    University of Wollongong)

  • Mark R. Davies

    (The University of Queensland
    The University of Melbourne)

  • Mark J. Walker

    (The University of Queensland)

Abstract

The re-emergence of scarlet fever poses a new global public health threat. The capacity of North-East Asian serotype M12 (emm12) Streptococcus pyogenes (group A Streptococcus, GAS) to cause scarlet fever has been linked epidemiologically to the presence of novel prophages, including prophage ΦHKU.vir encoding the secreted superantigens SSA and SpeC and the DNase Spd1. Here, we report the molecular characterization of ΦHKU.vir-encoded exotoxins. We demonstrate that streptolysin O (SLO)-induced glutathione efflux from host cellular stores is a previously unappreciated GAS virulence mechanism that promotes SSA release and activity, representing the first description of a thiol-activated bacterial superantigen. Spd1 is required for resistance to neutrophil killing. Investigating single, double and triple isogenic knockout mutants of the ΦHKU.vir-encoded exotoxins, we find that SpeC and Spd1 act synergistically to facilitate nasopharyngeal colonization in a mouse model. These results offer insight into the pathogenesis of scarlet fever-causing GAS mediated by prophage ΦHKU.vir exotoxins.

Suggested Citation

  • Stephan Brouwer & Timothy C. Barnett & Diane Ly & Katherine J. Kasper & David M. P. Oliveira & Tania Rivera-Hernandez & Amanda J. Cork & Liam McIntyre & Magnus G. Jespersen & Johanna Richter & Benjami, 2020. "Prophage exotoxins enhance colonization fitness in epidemic scarlet fever-causing Streptococcus pyogenes," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18700-5
    DOI: 10.1038/s41467-020-18700-5
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    Cited by:

    1. M. Kalindu D. Rodrigo & Aarti Saiganesh & Andrew J. Hayes & Alisha M. Wilson & Jack Anstey & Janessa L. Pickering & Jua Iwasaki & Jessica Hillas & Scott Winslow & Tabitha Woodman & Philipp Nitschke & , 2022. "Host-dependent resistance of Group A Streptococcus to sulfamethoxazole mediated by a horizontally-acquired reduced folate transporter," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Mark R. Davies & Nadia Keller & Stephan Brouwer & Magnus G. Jespersen & Amanda J. Cork & Andrew J. Hayes & Miranda E. Pitt & David M. P. Oliveira & Nichaela Harbison-Price & Olivia M. Bertolla & Danie, 2023. "Detection of Streptococcus pyogenes M1UK in Australia and characterization of the mutation driving enhanced expression of superantigen SpeA," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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