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Communication between viruses guides lysis–lysogeny decisions

Author

Listed:
  • Zohar Erez

    (Weizmann Institute of Science)

  • Ida Steinberger-Levy

    (Weizmann Institute of Science
    Israel Institute for Biological Research)

  • Maya Shamir

    (Weizmann Institute of Science)

  • Shany Doron

    (Weizmann Institute of Science)

  • Avigail Stokar-Avihail

    (Weizmann Institute of Science)

  • Yoav Peleg

    (Israel Structural Proteomics Center (ISPC), Faculty of Biochemistry, Weizmann Institute of Science)

  • Sarah Melamed

    (Weizmann Institute of Science)

  • Azita Leavitt

    (Weizmann Institute of Science)

  • Alon Savidor

    (de Botton Institute for Protein Profiling, The Nancy and Stephen Grand Israel National Center for Personalized Medicine, Weizmann Institute of Science)

  • Shira Albeck

    (Israel Structural Proteomics Center (ISPC), Faculty of Biochemistry, Weizmann Institute of Science)

  • Gil Amitai

    (Weizmann Institute of Science)

  • Rotem Sorek

    (Weizmann Institute of Science)

Abstract

Temperate viruses can become dormant in their host cells, a process called lysogeny. In every infection, such viruses decide between the lytic and the lysogenic cycles, that is, whether to replicate and lyse their host or to lysogenize and keep the host viable. Here we show that viruses (phages) of the SPbeta group use a small-molecule communication system to coordinate lysis–lysogeny decisions. During infection of its Bacillus host cell, the phage produces a six amino-acids-long communication peptide that is released into the medium. In subsequent infections, progeny phages measure the concentration of this peptide and lysogenize if the concentration is sufficiently high. We found that different phages encode different versions of the communication peptide, demonstrating a phage-specific peptide communication code for lysogeny decisions. We term this communication system the ‘arbitrium’ system, and further show that it is encoded by three phage genes: aimP, which produces the peptide; aimR, the intracellular peptide receptor; and aimX, a negative regulator of lysogeny. The arbitrium system enables a descendant phage to ‘communicate’ with its predecessors, that is, to estimate the amount of recent previous infections and hence decide whether to employ the lytic or lysogenic cycle.

Suggested Citation

  • Zohar Erez & Ida Steinberger-Levy & Maya Shamir & Shany Doron & Avigail Stokar-Avihail & Yoav Peleg & Sarah Melamed & Azita Leavitt & Alon Savidor & Shira Albeck & Gil Amitai & Rotem Sorek, 2017. "Communication between viruses guides lysis–lysogeny decisions," Nature, Nature, vol. 541(7638), pages 488-493, January.
  • Handle: RePEc:nat:nature:v:541:y:2017:i:7638:d:10.1038_nature21049
    DOI: 10.1038/nature21049
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    Citations

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    Cited by:

    1. Francisca Gallego del Sol & Nuria Quiles-Puchalt & Aisling Brady & José R. Penadés & Alberto Marina, 2022. "Insights into the mechanism of action of the arbitrium communication system in SPbeta phages," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Shengbo Wu & Jie Feng & Chunjiang Liu & Hao Wu & Zekai Qiu & Jianjun Ge & Shuyang Sun & Xia Hong & Yukun Li & Xiaona Wang & Aidong Yang & Fei Guo & Jianjun Qiao, 2022. "Machine learning aided construction of the quorum sensing communication network for human gut microbiota," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Angela Tung & Megan M. Sperry & Wesley Clawson & Ananya Pavuluri & Sydney Bulatao & Michelle Yue & Ramses Martinez Flores & Vaibhav P. Pai & Patrick McMillen & Franz Kuchling & Michael Levin, 2024. "Embryos assist morphogenesis of others through calcium and ATP signaling mechanisms in collective teratogen resistance," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    4. Koen Wortelboer & Patrick A. Jonge & Torsten P. M. Scheithauer & Ilias Attaye & E. Marleen Kemper & Max Nieuwdorp & Hilde Herrema, 2023. "Phage-microbe dynamics after sterile faecal filtrate transplantation in individuals with metabolic syndrome: a double-blind, randomised, placebo-controlled clinical trial assessing efficacy and safety," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Asher Leeks & Stuart A. West & Melanie Ghoul, 2021. "The evolution of cheating in viruses," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

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