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

Abstract
Data availability
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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

1. Lukasz Jaremko
(2020) Chemical shifts of H-NS C-term with linker
BMRB, 50239.

https://bmrb.io/data_library/summary/index.php?bmrbId=50239
1. Lukasz Jaremko
(2020) Chemical shifts of H-NS C-term with linker against the N-term site1
BMRB, 50240.

https://bmrb.io/data_library/summary/index.php?bmrbId=50240

Article and author information

Author details

Xiaochuan Zhao

Department of Chemistry, University of Vermont, Burlington, United States

Competing interests
The authors declare that no competing interests exist.
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.
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.
Chenyi Liao

Department of Chemistry, University of Vermont, Burlington, United States

Competing interests
The authors declare that no competing interests exist.
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.
Jacob M Remington

Department of Chemistry, University of Vermont, Burlington, United States

Competing interests
The authors declare that no competing interests exist.
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.
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.
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.
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.

"This ORCID iD identifies the author of this article:" 0000-0001-5278-0668
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.

"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.

Copyright

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.