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...

Full description

Bibliographic Details
Main Authors: Yan Yang, Guanpeng Xu, Jingdan Liang, Ying He, Lei Xiong, Hui Li, Douglas Bartlett, Zixin Deng, Zhijun Wang, Xiang Xiao
Format: Article
Language:English
Published: Nature Portfolio 2017-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-02445-1
_version_ 1818423226547568640
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.
first_indexed 2024-12-14T13:38:47Z
format Article
id doaj.art-1ff47aaf03a04b9eb534c3de6f7b364a
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-12-14T13:38:47Z
publishDate 2017-06-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
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
work_keys_str_mv AT yanyang dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction
AT guanpengxu dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction
AT jingdanliang dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction
AT yinghe dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction
AT leixiong dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction
AT huili dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction
AT douglasbartlett dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction
AT zixindeng dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction
AT zhijunwang dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction
AT xiangxiao dnabackbonesulfurmodificationexpandsmicrobialgrowthrangeundermultiplestressesbyitsantioxidationfunction