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The origin and impeded dissemination of the DNA phosphorothioation system in prokaryotes

Huahua Jian, Guanpeng Xu, Yi Yi, Yali Hao, Yinzhao Wang, Lei Xiong, Siyuan Wang, Shunzhang Liu, Canxing Meng, Jiahua Wang, Yue Zhang, Chao Chen, Xiaoyuan Feng, Haiwei Luo, Hao Zhang, Xingguo Zhang, Lianrong Wang, Zhijun Wang, Zixin Deng and Xiang Xiao ()
Additional contact information
Huahua Jian: Shanghai Jiao Tong University
Guanpeng Xu: Shanghai Jiao Tong University
Yi Yi: Shanghai Jiao Tong University
Yali Hao: Shanghai Jiao Tong University
Yinzhao Wang: Shanghai Jiao Tong University
Lei Xiong: Wuhan University
Siyuan Wang: Shanghai Jiao Tong University
Shunzhang Liu: Shanghai Jiao Tong University
Canxing Meng: Shanghai Jiao Tong University
Jiahua Wang: Shanghai Jiao Tong University
Yue Zhang: Shanghai Jiao Tong University
Chao Chen: Wuhan University
Xiaoyuan Feng: Shanghai Jiao Tong University
Haiwei Luo: The Chinese University of Hong Kong
Hao Zhang: The Chinese University of Hong Kong
Xingguo Zhang: Grandomics Biosciences
Lianrong Wang: Wuhan University
Zhijun Wang: Shanghai Jiao Tong University
Zixin Deng: Shanghai Jiao Tong University
Xiang Xiao: Shanghai Jiao Tong University

Nature Communications, 2021, vol. 12, issue 1, 1-16

Abstract: Abstract Phosphorothioate (PT) modification by the dnd gene cluster is the first identified DNA backbone modification and constitute an epigenetic system with multiple functions, including antioxidant ability, restriction modification, and virus resistance. Despite these advantages for hosting dnd systems, they are surprisingly distributed sporadically among contemporary prokaryotic genomes. To address this ecological paradox, we systematically investigate the occurrence and phylogeny of dnd systems, and they are suggested to have originated in ancient Cyanobacteria after the Great Oxygenation Event. Interestingly, the occurrence of dnd systems and prophages is significantly negatively correlated. Further, we experimentally confirm that PT modification activates the filamentous phage SW1 by altering the binding affinity of repressor and the transcription level of its encoding gene. Competition assays, concurrent epigenomic and transcriptomic sequencing subsequently show that PT modification affects the expression of a variety of metabolic genes, which reduces the competitive fitness of the marine bacterium Shewanella piezotolerans WP3. Our findings strongly suggest that a series of negative effects on microorganisms caused by dnd systems limit horizontal gene transfer, thus leading to their sporadic distribution. Overall, our study reveals putative evolutionary scenario of the dnd system and provides novel insights into the physiological and ecological influences of PT modification.

Date: 2021
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DOI: 10.1038/s41467-021-26636-7

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