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Molecular Pathogenesis | Spotlight

Phosphotransferase System Uptake and Metabolism of the β-Glucoside Salicin Impact Group A Streptococcal Bloodstream Survival and Soft Tissue Infection

Rezia Era Braza, Aliyah B. Silver, Ganesh S. Sundar, Sarah E. Davis, Afrooz Razi, Emrul Islam, Meaghan Hart, Jinyi Zhu, Yoann Le Breton, Kevin S. McIver
Victor J. Torres, Editor
Rezia Era Braza
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Aliyah B. Silver
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Ganesh S. Sundar
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Sarah E. Davis
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Afrooz Razi
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Emrul Islam
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Meaghan Hart
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Jinyi Zhu
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Yoann Le Breton
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Kevin S. McIver
aDepartment of Cell Biology & Molecular Genetics, Maryland Pathogen Research Institute, University of Maryland, College Park, College Park, Maryland, USA
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Victor J. Torres
New York University School of Medicine
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DOI: 10.1128/IAI.00346-20
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ABSTRACT

Streptococcus pyogenes (group A Streptococcus [GAS]), a major human-specific pathogen, relies on efficient nutrient acquisition for successful infection within its host. The phosphotransferase system (PTS) couples the import of carbohydrates with their phosphorylation prior to metabolism and has been linked to GAS pathogenesis. In a screen of an insertional mutant library of all 14 annotated PTS permease (EIIC) genes in MGAS5005, the annotated β-glucoside PTS transporter (bglP) was found to be crucial for GAS growth and survival in human blood and was validated in another M1T1 GAS strain, 5448. In 5448, bglP was shown to be in an operon with a putative phospho-β-glucosidase (bglB) downstream and a predicted antiterminator (licT) upstream. Using defined nonpolar mutants of the β-glucoside permease (bglP) and β-glucosidase enzyme (bglB) in 5448, we showed that bglB, not bglP, was important for growth in blood. Furthermore, transcription of the licT-blgPB operon was found to be repressed by glucose and induced by the β-glucoside salicin as the sole carbon source. Investigation of the individual bglP and bglB mutants determined that they influence in vitro growth in the β-glucoside salicin; however, only bglP was necessary for growth in other non-β-glucoside PTS sugars, such as fructose and mannose. Additionally, loss of BglP and BglB suggests that they are important for the regulation of virulence-related genes that control biofilm formation, streptolysin S (SLS)-mediated hemolysis, and localized ulcerative lesion progression during subcutaneous infections in mice. Thus, our results indicate that the β-glucoside PTS transports salicin and its metabolism can differentially influence GAS pathophysiology during soft tissue infection.

FOOTNOTES

    • Received 12 June 2020.
    • Returned for modification 6 July 2020.
    • Accepted 22 July 2020.
    • Accepted manuscript posted online 27 July 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Phosphotransferase System Uptake and Metabolism of the β-Glucoside Salicin Impact Group A Streptococcal Bloodstream Survival and Soft Tissue Infection
Rezia Era Braza, Aliyah B. Silver, Ganesh S. Sundar, Sarah E. Davis, Afrooz Razi, Emrul Islam, Meaghan Hart, Jinyi Zhu, Yoann Le Breton, Kevin S. McIver
Infection and Immunity Sep 2020, 88 (10) e00346-20; DOI: 10.1128/IAI.00346-20

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Phosphotransferase System Uptake and Metabolism of the β-Glucoside Salicin Impact Group A Streptococcal Bloodstream Survival and Soft Tissue Infection
Rezia Era Braza, Aliyah B. Silver, Ganesh S. Sundar, Sarah E. Davis, Afrooz Razi, Emrul Islam, Meaghan Hart, Jinyi Zhu, Yoann Le Breton, Kevin S. McIver
Infection and Immunity Sep 2020, 88 (10) e00346-20; DOI: 10.1128/IAI.00346-20
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KEYWORDS

β-glucoside
GAS pathophysiology
GAS metabolism
PTS systems
virulence regulation

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