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Molecular Pathogenesis

Intergenic Variable-Number Tandem-Repeat Polymorphism Upstream of rocA Alters Toxin Production and Enhances Virulence in Streptococcus pyogenes

Luchang Zhu, Randall J. Olsen, Nicola Horstmann, Samuel A. Shelburne, Jia Fan, Ye Hu, James M. Musser
A. Camilli, Editor
Luchang Zhu
aCenter for Molecular and Translational Human Infectious Diseases Research, Houston Methodist Research Institute, and Department of Pathology and Genomic Medicine, Houston Methodist Hospital, Houston, Texas, USA
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Randall J. Olsen
aCenter for Molecular and Translational Human Infectious Diseases Research, Houston Methodist Research Institute, and Department of Pathology and Genomic Medicine, Houston Methodist Hospital, Houston, Texas, USA
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Nicola Horstmann
bDepartment of Infectious Diseases, MD Anderson Cancer Center, Houston, Texas, USA
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Samuel A. Shelburne
bDepartment of Infectious Diseases, MD Anderson Cancer Center, Houston, Texas, USA
cDepartment of Genomic Medicine, MD Anderson Cancer Center, Houston, Texas, USA
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Jia Fan
dDepartment of Nanomedicine, Houston Methodist Research Institute, Houston, Texas, USA
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Ye Hu
dDepartment of Nanomedicine, Houston Methodist Research Institute, Houston, Texas, USA
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James M. Musser
aCenter for Molecular and Translational Human Infectious Diseases Research, Houston Methodist Research Institute, and Department of Pathology and Genomic Medicine, Houston Methodist Hospital, Houston, Texas, USA
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A. Camilli
Tufts University School of Medicine
Roles: Editor
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DOI: 10.1128/IAI.00258-16
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ABSTRACT

Variable-number tandem-repeat (VNTR) polymorphisms are ubiquitous in bacteria. However, only a small fraction of them has been functionally studied. Here, we report an intergenic VNTR polymorphism that confers an altered level of toxin production and increased virulence in Streptococcus pyogenes. The nature of the polymorphism is a one-unit deletion in a three-tandem-repeat locus upstream of the rocA gene encoding a sensor kinase. S. pyogenes strains with this type of polymorphism cause human infection and produce significantly larger amounts of the secreted cytotoxins S. pyogenes NADase (SPN) and streptolysin O (SLO). Using isogenic mutant strains, we demonstrate that deleting one or more units of the tandem repeats abolished RocA production, reduced CovR phosphorylation, derepressed multiple CovR-regulated virulence factors (such as SPN and SLO), and increased virulence in a mouse model of necrotizing fasciitis. The phenotypic effect of the VNTR polymorphism was nearly the same as that of inactivating the rocA gene. In summary, we identified and characterized an intergenic VNTR polymorphism in S. pyogenes that affects toxin production and virulence. These new findings enhance understanding of rocA biology and the function of VNTR polymorphisms in S. pyogenes.

FOOTNOTES

    • Received 24 March 2016.
    • Returned for modification 17 April 2016.
    • Accepted 26 April 2016.
    • Accepted manuscript posted online 2 May 2016.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/IAI.00258-16.

  • Copyright © 2016, American Society for Microbiology. All Rights Reserved.
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Intergenic Variable-Number Tandem-Repeat Polymorphism Upstream of rocA Alters Toxin Production and Enhances Virulence in Streptococcus pyogenes
Luchang Zhu, Randall J. Olsen, Nicola Horstmann, Samuel A. Shelburne, Jia Fan, Ye Hu, James M. Musser
Infection and Immunity Jun 2016, 84 (7) 2086-2093; DOI: 10.1128/IAI.00258-16

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Intergenic Variable-Number Tandem-Repeat Polymorphism Upstream of rocA Alters Toxin Production and Enhances Virulence in Streptococcus pyogenes
Luchang Zhu, Randall J. Olsen, Nicola Horstmann, Samuel A. Shelburne, Jia Fan, Ye Hu, James M. Musser
Infection and Immunity Jun 2016, 84 (7) 2086-2093; DOI: 10.1128/IAI.00258-16
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