IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26636-7.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26636-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-26636-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Meishun Yu & Menghui Zhang & Runying Zeng & Ruolin Cheng & Rui Zhang & Yanping Hou & Fangfang Kuang & Xuejin Feng & Xiyang Dong & Yinfang Li & Zongze Shao & Min Jin, 2024. "Diversity and potential host-interactions of viruses inhabiting deep-sea seamount sediments," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Ngat T. Tran & Tung B. K. Le, 2024. "Control of a gene transfer agent cluster in Caulobacter crescentus by transcriptional activation and anti-termination," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Krishna, Shubham & Peterson, Victoria & Listmann, Luisa & Hinners, Jana, 2024. "Interactive effects of viral lysis and warming in a coastal ocean identified from an idealized ecosystem model," Ecological Modelling, Elsevier, vol. 487(C).
    4. Xuan Zou & Xiaohong Xiao & Ziran Mo & Yashi Ge & Xing Jiang & Ruolin Huang & Mengxue Li & Zixin Deng & Shi Chen & Lianrong Wang & Sang Yup Lee, 2022. "Systematic strategies for developing phage resistant Escherichia coli strains," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26636-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.