1. Biochemistry and Chemical Biology
  2. Computational and Systems Biology

Molecular basis for the adaptive evolution of environment sensing by H-NS proteins

  1. Xiaochuan Zhao
  2. Umar Farook Shahul Hameed
  3. Vladlena Kharchenko
  4. Chenyi Liao
  5. Franceline Huser
  6. Jacob M Remington
  7. Anand K Radhakrishnan
  8. Mariusz Jaremko
  9. Łukasz Jaremko  Is a corresponding author
  10. Stefan T Arold  Is a corresponding author
  11. Jianing Li  Is a corresponding author
  1. University of Vermont, United States
  2. King Abdullah University of Science and Technology, Saudi Arabia
https://doi.org/10.7554/eLife.57467
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Cite this article
  1. Xiaochuan Zhao
  2. Umar Farook Shahul Hameed
  3. Vladlena Kharchenko
  4. Chenyi Liao
  5. Franceline Huser
  6. Jacob M Remington
  7. Anand K Radhakrishnan
  8. Mariusz Jaremko
  9. Łukasz Jaremko
  10. Stefan T Arold
  11. Jianing Li
(2021)
Molecular basis for the adaptive evolution of environment sensing by H-NS proteins
eLife 10:e57467.
https://doi.org/10.7554/eLife.57467
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Abstract

The DNA-binding protein H-NS is a pleiotropic gene regulator in gram-negative bacteria. Through its capacity to sense temperature and other environmental factors, H-NS allows pathogens like Salmonella to adapt their gene expression to their presence inside or outside warm-blooded hosts. To investigate how this sensing mechanism may have evolved to fit different bacterial lifestyles, we compared H-NS orthologs from bacteria that infect humans, plants, and insects, and from bacteria that live on a deep-sea hypothermal vent. The combination of biophysical characterization, high-resolution proton-less NMR spectroscopy and molecular simulations revealed, at an atomistic level, how the same general mechanism was adapted to specific habitats and lifestyles. In particular, we demonstrate how environment-sensing characteristics arise from specifically positioned intra- or intermolecular electrostatic interactions. Our integrative approach clarified the exact modus operandi for H-NS–mediated environmental sensing and suggests that this sensing mechanism resulted from the exaptation of an ancestral protein feature.

Data availability

NMR chemical shift assignments were deposited at the BMBR https://betadeposit.bmrb.wisc.edu/ with IDs 50239 and 50240

The following data sets were generated

Article and author information

Author details

  1. Xiaochuan Zhao

    Department of Chemistry, University of Vermont, Burlington, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Umar Farook Shahul Hameed

    Computational Bioscience Research Center; Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
    Competing interests
    The authors declare that no competing interests exist.

  3. Vladlena Kharchenko

    Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
    Competing interests
    The authors declare that no competing interests exist.

  4. Chenyi Liao

    Department of Chemistry, University of Vermont, Burlington, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Franceline Huser

    Computational Bioscience Research Center; Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
    Competing interests
    The authors declare that no competing interests exist.

  6. Jacob M Remington

    Department of Chemistry, University of Vermont, Burlington, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Anand K Radhakrishnan

    Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
    Competing interests
    The authors declare that no competing interests exist.

  8. Mariusz Jaremko

    Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
    Competing interests
    The authors declare that no competing interests exist.

  9. Łukasz Jaremko

    Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
    For correspondence
    lukasz.jaremko@kaust.edu.sa
    Competing interests
    The authors declare that no competing interests exist.

  10. Stefan T Arold

    Computational Bioscience Research Center; Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
    For correspondence
    stefan.arold@kaust.edu.sa
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5278-0668

  11. Jianing Li

    Department of Chemistry, University of Vermont, Burlington, United States
    For correspondence
    jianing.li@uvm.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0143-8894

Funding

King Abdullah University of Science and Technology (FCC/1/1976-25)

  • Xiaochuan Zhao

National Institute of General Medical Sciences (R01GM129431)

  • Jianing Li

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Yibing Shan, Antidote Health Foundation, United States

Publication history

  1. Received: April 1, 2020
  2. Accepted: January 6, 2021
  3. Accepted Manuscript published: January 7, 2021 (version 1)
  4. Version of Record published: January 20, 2021 (version 2)

Copyright

© 2021, Zhao et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Xiaochuan Zhao
  2. Umar Farook Shahul Hameed
  3. Vladlena Kharchenko
  4. Chenyi Liao
  5. Franceline Huser
  6. Jacob M Remington
  7. Anand K Radhakrishnan
  8. Mariusz Jaremko
  9. Łukasz Jaremko
  10. Stefan T Arold
  11. Jianing Li
(2021)
Molecular basis for the adaptive evolution of environment sensing by H-NS proteins
eLife 10:e57467.
https://doi.org/10.7554/eLife.57467

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