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

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 investiga...

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Main Authors: Xiaochuan Zhao, Umar F Shahul Hameed, Vladlena Kharchenko, Chenyi Liao, Franceline Huser, Jacob M Remington, Anand K Radhakrishnan, Mariusz Jaremko, Łukasz Jaremko, Stefan T Arold, Jianing Li
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/57467
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spelling doaj-3fd228bea29d480e96df7597f5c5d48b2021-05-05T22:39:49ZengeLife Sciences Publications LtdeLife2050-084X2021-01-011010.7554/eLife.57467Molecular basis for the adaptive evolution of environment-sensing by H-NS proteinsXiaochuan Zhao0https://orcid.org/0000-0002-0127-4789Umar F Shahul Hameed1https://orcid.org/0000-0002-0552-7149Vladlena Kharchenko2Chenyi Liao3Franceline Huser4Jacob M Remington5Anand K Radhakrishnan6Mariusz Jaremko7Łukasz Jaremko8https://orcid.org/0000-0001-7684-9359Stefan T Arold9https://orcid.org/0000-0001-5278-0668Jianing Li10https://orcid.org/0000-0002-0143-8894Department of Chemistry, The University of Vermont, Burlington, United StatesKing Abdullah University of Science and Technology (KAUST), Computational Bioscience Research Center (CBRC), Biological and Environmental Science and Engineering (BESE), Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering (BESE), Thuwal, Saudi ArabiaDepartment of Chemistry, The University of Vermont, Burlington, United StatesKing Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering (BESE), Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering (BESE), Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering (BESE), Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering (BESE), Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering (BESE), Thuwal, Saudi ArabiaKing Abdullah University of Science and Technology (KAUST), Computational Bioscience Research Center (CBRC), Biological and Environmental Science and Engineering (BESE), Thuwal, Saudi Arabia; Centre de Biochimie Structurale, CNRS, INSERM, Université de Montpellier, Montpellier, FranceDepartment of Chemistry, The University of Vermont, Burlington, United StatesThe 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 nuclear magnetic resonance 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 suggested that this sensing mechanism resulted from the exaptation of an ancestral protein feature.https://elifesciences.org/articles/57467salmonella typhimuriumerwinia amylovorabuchnera aphidicolaidiomarina loiheinsisevolutionenvironment-sensing
collection DOAJ
language English
format Article
sources DOAJ
author Xiaochuan Zhao
Umar F Shahul Hameed
Vladlena Kharchenko
Chenyi Liao
Franceline Huser
Jacob M Remington
Anand K Radhakrishnan
Mariusz Jaremko
Łukasz Jaremko
Stefan T Arold
Jianing Li
spellingShingle Xiaochuan Zhao
Umar F Shahul Hameed
Vladlena Kharchenko
Chenyi Liao
Franceline Huser
Jacob M Remington
Anand K Radhakrishnan
Mariusz Jaremko
Łukasz Jaremko
Stefan T Arold
Jianing Li
Molecular basis for the adaptive evolution of environment-sensing by H-NS proteins
eLife
salmonella typhimurium
erwinia amylovora
buchnera aphidicola
idiomarina loiheinsis
evolution
environment-sensing
author_facet Xiaochuan Zhao
Umar F Shahul Hameed
Vladlena Kharchenko
Chenyi Liao
Franceline Huser
Jacob M Remington
Anand K Radhakrishnan
Mariusz Jaremko
Łukasz Jaremko
Stefan T Arold
Jianing Li
author_sort Xiaochuan Zhao
title Molecular basis for the adaptive evolution of environment-sensing by H-NS proteins
title_short Molecular basis for the adaptive evolution of environment-sensing by H-NS proteins
title_full Molecular basis for the adaptive evolution of environment-sensing by H-NS proteins
title_fullStr Molecular basis for the adaptive evolution of environment-sensing by H-NS proteins
title_full_unstemmed Molecular basis for the adaptive evolution of environment-sensing by H-NS proteins
title_sort molecular basis for the adaptive evolution of environment-sensing by h-ns proteins
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-01-01
description 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 nuclear magnetic resonance 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 suggested that this sensing mechanism resulted from the exaptation of an ancestral protein feature.
topic salmonella typhimurium
erwinia amylovora
buchnera aphidicola
idiomarina loiheinsis
evolution
environment-sensing
url https://elifesciences.org/articles/57467
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