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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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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