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Reduced Protein Synthesis Fidelity Inhibits Flagellar Biosynthesis and Motility

Accurate translation of the genetic information from DNA to protein is maintained by multiple quality control steps from bacteria to mammals. Genetic and environmental alterations have been shown to compromise translational quality control and reduce fidelity during protein synthesis. The physiologi...

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Autores principales: Fan, Yongqiang, Evans, Christopher R., Ling, Jiqiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4965754/
https://www.ncbi.nlm.nih.gov/pubmed/27468805
http://dx.doi.org/10.1038/srep30960
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author Fan, Yongqiang
Evans, Christopher R.
Ling, Jiqiang
author_facet Fan, Yongqiang
Evans, Christopher R.
Ling, Jiqiang
author_sort Fan, Yongqiang
collection PubMed
description Accurate translation of the genetic information from DNA to protein is maintained by multiple quality control steps from bacteria to mammals. Genetic and environmental alterations have been shown to compromise translational quality control and reduce fidelity during protein synthesis. The physiological impact of increased translational errors is not fully understood. While generally considered harmful, translational errors have recently been shown to benefit cells under certain stress conditions. In this work, we describe a novel regulatory pathway in which reduced translational fidelity downregulates expression of flagellar genes and suppresses bacterial motility. Electron microscopy imaging shows that the error-prone Escherichia coli strain lacks mature flagella. Further genetic analyses reveal that translational errors upregulate expression of a small RNA DsrA through enhancing its transcription, and deleting DsrA from the error-prone strain restores motility. DsrA regulates expression of H-NS and RpoS, both of which regulate flagellar genes. We demonstrate that an increased level of DsrA in the error-prone strain suppresses motility through the H-NS pathway. Our work suggests that bacteria are capable of switching on and off the flagellar system by altering translational fidelity, which may serve as a previously unknown mechanism to improve fitness in response to environmental cues.
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spelling pubmed-49657542016-08-08 Reduced Protein Synthesis Fidelity Inhibits Flagellar Biosynthesis and Motility Fan, Yongqiang Evans, Christopher R. Ling, Jiqiang Sci Rep Article Accurate translation of the genetic information from DNA to protein is maintained by multiple quality control steps from bacteria to mammals. Genetic and environmental alterations have been shown to compromise translational quality control and reduce fidelity during protein synthesis. The physiological impact of increased translational errors is not fully understood. While generally considered harmful, translational errors have recently been shown to benefit cells under certain stress conditions. In this work, we describe a novel regulatory pathway in which reduced translational fidelity downregulates expression of flagellar genes and suppresses bacterial motility. Electron microscopy imaging shows that the error-prone Escherichia coli strain lacks mature flagella. Further genetic analyses reveal that translational errors upregulate expression of a small RNA DsrA through enhancing its transcription, and deleting DsrA from the error-prone strain restores motility. DsrA regulates expression of H-NS and RpoS, both of which regulate flagellar genes. We demonstrate that an increased level of DsrA in the error-prone strain suppresses motility through the H-NS pathway. Our work suggests that bacteria are capable of switching on and off the flagellar system by altering translational fidelity, which may serve as a previously unknown mechanism to improve fitness in response to environmental cues. Nature Publishing Group 2016-07-29 /pmc/articles/PMC4965754/ /pubmed/27468805 http://dx.doi.org/10.1038/srep30960 Text en Copyright © 2016, The Author(s) http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Fan, Yongqiang
Evans, Christopher R.
Ling, Jiqiang
Reduced Protein Synthesis Fidelity Inhibits Flagellar Biosynthesis and Motility
title Reduced Protein Synthesis Fidelity Inhibits Flagellar Biosynthesis and Motility
title_full Reduced Protein Synthesis Fidelity Inhibits Flagellar Biosynthesis and Motility
title_fullStr Reduced Protein Synthesis Fidelity Inhibits Flagellar Biosynthesis and Motility
title_full_unstemmed Reduced Protein Synthesis Fidelity Inhibits Flagellar Biosynthesis and Motility
title_short Reduced Protein Synthesis Fidelity Inhibits Flagellar Biosynthesis and Motility
title_sort reduced protein synthesis fidelity inhibits flagellar biosynthesis and motility
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4965754/
https://www.ncbi.nlm.nih.gov/pubmed/27468805
http://dx.doi.org/10.1038/srep30960
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