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Promiscuity of response regulators for thioredoxin steers bacterial virulence

Author

Listed:
  • Ju-Sim Kim

    (University of Colorado School of Medicine, Department of Immunology & Microbiology)

  • Alexandra Born

    (University of Colorado School of Medicine, Department of Biochemistry & Molecular Genetics)

  • James Karl A. Till

    (University of Colorado School of Medicine, Department of Immunology & Microbiology)

  • Lin Liu

    (University of Colorado School of Medicine, Department of Immunology & Microbiology)

  • Sashi Kant

    (University of Colorado School of Medicine, Department of Immunology & Microbiology)

  • Morkos A. Henen

    (University of Colorado School of Medicine, Department of Biochemistry & Molecular Genetics
    Mansoura University)

  • Beat Vögeli

    (University of Colorado School of Medicine, Department of Biochemistry & Molecular Genetics)

  • Andrés Vázquez-Torres

    (University of Colorado School of Medicine, Department of Immunology & Microbiology
    Veterans Affairs Eastern Colorado Health Care System)

Abstract

The exquisite specificity between a sensor kinase and its cognate response regulator ensures faithful partner selectivity within two-component pairs concurrently firing in a single bacterium, minimizing crosstalk with other members of this conserved family of paralogous proteins. We show that conserved hydrophobic and charged residues on the surface of thioredoxin serve as a docking station for structurally diverse response regulators. Using the OmpR protein, we identify residues in the flexible linker and the C-terminal β-hairpin that enable associations of this archetypical response regulator with thioredoxin, but are dispensable for interactions of this transcription factor to its cognate sensor kinase EnvZ, DNA or RNA polymerase. Here we show that the promiscuous interactions of response regulators with thioredoxin foster the flow of information through otherwise highly dedicated two-component signaling systems, thereby enabling both the transcription of Salmonella pathogenicity island-2 genes as well as growth of this intracellular bacterium in macrophages and mice.

Suggested Citation

  • Ju-Sim Kim & Alexandra Born & James Karl A. Till & Lin Liu & Sashi Kant & Morkos A. Henen & Beat Vögeli & Andrés Vázquez-Torres, 2022. "Promiscuity of response regulators for thioredoxin steers bacterial virulence," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33983-6
    DOI: 10.1038/s41467-022-33983-6
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    References listed on IDEAS

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    1. W. Ryan Will & Denise H. Bale & Philip J. Reid & Stephen J. Libby & Ferric C. Fang, 2014. "Evolutionary expansion of a regulatory network by counter-silencing," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    2. Sylvie Doublié & Stanley Tabor & Alexander M. Long & Charles C. Richardson & Tom Ellenberger, 1998. "Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution," Nature, Nature, vol. 391(6664), pages 251-258, January.
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