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

Author

Listed:
  • Huahua Jian

    (Shanghai Jiao Tong University
    Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai))

  • 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
    The Chinese University of Hong Kong)

  • 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
    Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai))

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.

Suggested Citation

  • 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 & Xi, 2021. "The origin and impeded dissemination of the DNA phosphorothioation system in prokaryotes," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26636-7
    DOI: 10.1038/s41467-021-26636-7
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    References listed on IDEAS

    as
    1. Lei Xiong & Siyi Liu & Si Chen & Yao Xiao & Bochen Zhu & Yali Gao & Yujing Zhang & Beibei Chen & Jie Luo & Zixin Deng & Xiangdong Chen & Lianrong Wang & Shi Chen, 2019. "A new type of DNA phosphorothioation-based antiviral system in archaea," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. Forest Rohwer & Rebecca Vega Thurber, 2009. "Viruses manipulate the marine environment," Nature, Nature, vol. 459(7244), pages 207-212, May.
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    Cited by:

    1. Yi Yi & Shunzhang Liu & Yali Hao & Qingyang Sun & Xinjuan Lei & Yecheng Wang & Jiahua Wang & Mujie Zhang & Shan Tang & Qingxue Tang & Yue Zhang & Xipeng Liu & Yinzhao Wang & Xiang Xiao & Huahua Jian, 2023. "A systematic analysis of marine lysogens and proviruses," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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