DNA Backbone Sulfur-Modification Expands Microbial Growth Range under Multiple Stresses by its anti-oxidation function
Abstract DNA phosphorothioate (PT) modification is a sulfur modification on the backbone of DNA introduced by the proteins DndA-E. It has been detected within many bacteria isolates and metagenomic datasets, including human pathogens, and is considered to be widely distributed in nature. However, li...
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Nature Portfolio
2017-06-01
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Series: | Scientific Reports |
Online Access: | https://doi.org/10.1038/s41598-017-02445-1 |
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author | Yan Yang Guanpeng Xu Jingdan Liang Ying He Lei Xiong Hui Li Douglas Bartlett Zixin Deng Zhijun Wang Xiang Xiao |
author_facet | Yan Yang Guanpeng Xu Jingdan Liang Ying He Lei Xiong Hui Li Douglas Bartlett Zixin Deng Zhijun Wang Xiang Xiao |
author_sort | Yan Yang |
collection | DOAJ |
description | Abstract DNA phosphorothioate (PT) modification is a sulfur modification on the backbone of DNA introduced by the proteins DndA-E. It has been detected within many bacteria isolates and metagenomic datasets, including human pathogens, and is considered to be widely distributed in nature. However, little is known about the physiological function of this modification, and thus its evolutionary significance and application potential remains largely a mystery. In this study, we focused on the advantages of DNA PT modification to bacterial cells coping with environmental stresses. We show that the mesophile Escherichia coli and the extremophile Shewanella piezotolerans both expanded their growth ranges following exposure to extreme temperature, salinity, pH, pressure, UV, X-ray and heavy metals as a result of DNA phophorothioation. The phophorothioated DNA reacted to both H2O2 and hydroxyl radicals in vivo, and protected genomic DNA as well as sensitive enzymes from intracellular oxidative damage. We further demonstrate that this process has evolved separate from its associated role in DNA restriction and modification. These findings provide a physiological role for a covalent modification widespread in nature and suggest possible applications in biotechnology and biomedicine. |
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issn | 2045-2322 |
language | English |
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spelling | doaj.art-1ff47aaf03a04b9eb534c3de6f7b364a2022-12-21T22:59:31ZengNature PortfolioScientific Reports2045-23222017-06-01711910.1038/s41598-017-02445-1DNA Backbone Sulfur-Modification Expands Microbial Growth Range under Multiple Stresses by its anti-oxidation functionYan Yang0Guanpeng Xu1Jingdan Liang2Ying He3Lei Xiong4Hui Li5Douglas Bartlett6Zixin Deng7Zhijun Wang8Xiang Xiao9State Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong UniversityCentral Analytical lab, School of Chemistry and Chemical Engineering, Shanghai Jiao Tong UniversityCenter for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San DiegoState Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong UniversityAbstract DNA phosphorothioate (PT) modification is a sulfur modification on the backbone of DNA introduced by the proteins DndA-E. It has been detected within many bacteria isolates and metagenomic datasets, including human pathogens, and is considered to be widely distributed in nature. However, little is known about the physiological function of this modification, and thus its evolutionary significance and application potential remains largely a mystery. In this study, we focused on the advantages of DNA PT modification to bacterial cells coping with environmental stresses. We show that the mesophile Escherichia coli and the extremophile Shewanella piezotolerans both expanded their growth ranges following exposure to extreme temperature, salinity, pH, pressure, UV, X-ray and heavy metals as a result of DNA phophorothioation. The phophorothioated DNA reacted to both H2O2 and hydroxyl radicals in vivo, and protected genomic DNA as well as sensitive enzymes from intracellular oxidative damage. We further demonstrate that this process has evolved separate from its associated role in DNA restriction and modification. These findings provide a physiological role for a covalent modification widespread in nature and suggest possible applications in biotechnology and biomedicine.https://doi.org/10.1038/s41598-017-02445-1 |
spellingShingle | Yan Yang Guanpeng Xu Jingdan Liang Ying He Lei Xiong Hui Li Douglas Bartlett Zixin Deng Zhijun Wang Xiang Xiao DNA Backbone Sulfur-Modification Expands Microbial Growth Range under Multiple Stresses by its anti-oxidation function Scientific Reports |
title | DNA Backbone Sulfur-Modification Expands Microbial Growth Range under Multiple Stresses by its anti-oxidation function |
title_full | DNA Backbone Sulfur-Modification Expands Microbial Growth Range under Multiple Stresses by its anti-oxidation function |
title_fullStr | DNA Backbone Sulfur-Modification Expands Microbial Growth Range under Multiple Stresses by its anti-oxidation function |
title_full_unstemmed | DNA Backbone Sulfur-Modification Expands Microbial Growth Range under Multiple Stresses by its anti-oxidation function |
title_short | DNA Backbone Sulfur-Modification Expands Microbial Growth Range under Multiple Stresses by its anti-oxidation function |
title_sort | dna backbone sulfur modification expands microbial growth range under multiple stresses by its anti oxidation function |
url | https://doi.org/10.1038/s41598-017-02445-1 |
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