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Molecular Pathogenesis

Distinct Roles of the Salmonella enterica Serovar Typhimurium CyaY and YggX Proteins in the Biosynthesis and Repair of Iron-Sulfur Clusters

Jyoti Velayudhan, Joyce E. Karlinsey, Elaine R. Frawley, Lynne A. Becker, Margaret Nartea, Ferric C. Fang
S. M. Payne, Editor
Jyoti Velayudhan
aDepartment of Laboratory Medicine, University of Washington School of Medicine, Seattle, Washington, USA
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Joyce E. Karlinsey
bDepartment of Microbiology, University of Washington School of Medicine, Seattle, Washington, USA
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Elaine R. Frawley
aDepartment of Laboratory Medicine, University of Washington School of Medicine, Seattle, Washington, USA
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Lynne A. Becker
aDepartment of Laboratory Medicine, University of Washington School of Medicine, Seattle, Washington, USA
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Margaret Nartea
aDepartment of Laboratory Medicine, University of Washington School of Medicine, Seattle, Washington, USA
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Ferric C. Fang
aDepartment of Laboratory Medicine, University of Washington School of Medicine, Seattle, Washington, USA
bDepartment of Microbiology, University of Washington School of Medicine, Seattle, Washington, USA
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S. M. Payne
Roles: Editor
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DOI: 10.1128/IAI.01022-13
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ABSTRACT

Labile [4Fe-4S]2+ clusters found at the active sites of many dehydratases are susceptible to damage by univalent oxidants that convert the clusters to an inactive [3Fe-4S]1+ form. Bacteria repair damaged clusters in a process that does not require de novo protein synthesis or the Isc and Suf cluster assembly pathways. The current study investigates the participation of the bacterial frataxin ortholog CyaY and the YggX protein, which are proposed to play roles in iron trafficking and iron-sulfur cluster repair. Previous reports found that individual mutations in cyaY or yggX were not associated with phenotypic changes in Escherichia coli and Salmonella enterica serovar Typhimurium, suggesting that CyaY and YggX might have functionally redundant roles. However, we have found that individual mutations in cyaY or yggX confer enhanced susceptibility to hydrogen peroxide in Salmonella enterica serovar Typhimurium. In addition, inactivation of the stm3944 open reading frame, which is located immediately upstream of cyaY and which encodes a putative inner membrane protein, dramatically enhances the hydrogen peroxide sensitivity of a cyaY mutant. Overexpression of STM3944 reduces the elevated intracellular free iron levels observed in an S. Typhimurium fur mutant and also reduces the total cellular iron content under conditions of iron overload, suggesting that the stm3944-encoded protein may mediate iron efflux. Mutations in cyaY and yggX have different effects on the activities of the iron-sulfur cluster-containing aconitase, serine deaminase, and NADH dehydrogenase I enzymes of S. Typhimurium under basal conditions or following recovery from oxidative stress. In addition, cyaY and yggX mutations have additive effects on 6-phosphogluconate dehydratase-dependent growth during nitrosative stress, and a cyaY mutation reduces Salmonella virulence in mice. Collectively, these results indicate that CyaY and YggX play distinct supporting roles in iron-sulfur cluster biosynthesis and the repair of labile clusters damaged by univalent oxidants. Salmonella experiences oxidative and nitrosative stress within host phagocytes, and CyaY-dependent maintenance of labile iron-sulfur clusters appears to be important for Salmonella virulence.

FOOTNOTES

    • Received 16 August 2013.
    • Returned for modification 15 September 2013.
    • Accepted 22 December 2013.
    • Accepted manuscript posted online 13 January 2014.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/IAI.01022-13.

  • Copyright © 2014, American Society for Microbiology. All Rights Reserved.
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Distinct Roles of the Salmonella enterica Serovar Typhimurium CyaY and YggX Proteins in the Biosynthesis and Repair of Iron-Sulfur Clusters
Jyoti Velayudhan, Joyce E. Karlinsey, Elaine R. Frawley, Lynne A. Becker, Margaret Nartea, Ferric C. Fang
Infection and Immunity Mar 2014, 82 (4) 1390-1401; DOI: 10.1128/IAI.01022-13

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Distinct Roles of the Salmonella enterica Serovar Typhimurium CyaY and YggX Proteins in the Biosynthesis and Repair of Iron-Sulfur Clusters
Jyoti Velayudhan, Joyce E. Karlinsey, Elaine R. Frawley, Lynne A. Becker, Margaret Nartea, Ferric C. Fang
Infection and Immunity Mar 2014, 82 (4) 1390-1401; DOI: 10.1128/IAI.01022-13
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