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c-di-GMP inhibits the DNA binding activity of H-NS in Salmonella

Author

Listed:
  • Shuyu Li

    (Northwest A&F University)

  • Qinmeng Liu

    (Northwest A&F University)

  • Chongyi Duan

    (Northwest A&F University)

  • Jialin Li

    (Northwest A&F University)

  • Hengxi Sun

    (Northwest A&F University)

  • Lei Xu

    (Northwest A&F University)

  • Qiao Yang

    (Zhejiang Ocean University
    Donghai Laboratory)

  • Yao Wang

    (Northwest A&F University)

  • Xihui Shen

    (Northwest A&F University)

  • Lei Zhang

    (Northwest A&F University)

Abstract

Cyclic di-GMP (c-di-GMP) is a second messenger that transduces extracellular stimuli into cellular responses and regulates various biological processes in bacteria. H-NS is a global regulatory protein that represses expression of many genes, but how H-NS activity is modulated by environmental signals remains largely unclear. Here, we show that high intracellular c-di-GMP levels, induced by environmental cues, relieve H-NS-mediated transcriptional silencing in Salmonella enterica serovar Typhimurium. We find that c-di-GMP binds to the H-NS protein to inhibit its binding to DNA, thus derepressing genes silenced by H-NS. However, c-di-GMP is unable to displace H-NS from DNA. In addition, a K107A mutation in H-NS abolishes response to c-di-GMP but leaves its DNA binding activity unaffected in vivo. Our results thus suggest a mechanism by which H-NS acts as an environment-sensing regulator in Gram-negative bacteria.

Suggested Citation

  • Shuyu Li & Qinmeng Liu & Chongyi Duan & Jialin Li & Hengxi Sun & Lei Xu & Qiao Yang & Yao Wang & Xihui Shen & Lei Zhang, 2023. "c-di-GMP inhibits the DNA binding activity of H-NS in Salmonella," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43442-5
    DOI: 10.1038/s41467-023-43442-5
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    References listed on IDEAS

    as
    1. Remus T. Dame & Maarten C. Noom & Gijs J. L. Wuite, 2006. "Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation," Nature, Nature, vol. 444(7117), pages 387-390, November.
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    3. Weihui Li & Tao Cui & Lihua Hu & Ziqing Wang & Zongqiang Li & Zheng-Guo He, 2015. "Cyclic diguanylate monophosphate directly binds to human siderocalin and inhibits its antibacterial activity," Nature Communications, Nature, vol. 6(1), pages 1-9, November.
    4. Shuyu Li & Hengxi Sun & Jianghan Li & Yujiao Zhao & Ruiying Wang & Lei Xu & Chongyi Duan & Jialin Li & Zhuo Wang & Qinmeng Liu & Yao Wang & Songying Ouyang & Xihui Shen & Lei Zhang, 2022. "Autoinducer-2 and bile salts induce c-di-GMP synthesis to repress the T3SS via a T3SS chaperone," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
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    6. Li Song & Junfeng Pan & Yantao Yang & Zhenxing Zhang & Rui Cui & Shuangkai Jia & Zhuo Wang & Changxing Yang & Lei Xu & Tao G. Dong & Yao Wang & Xihui Shen, 2021. "Contact-independent killing mediated by a T6SS effector with intrinsic cell-entry properties," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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