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An inorganic mineral-based protocell with prebiotic radiation fitness

Author

Listed:
  • Shang Dai

    (Zhejiang University
    Shanghai Institute for Advanced Study of Zhejiang University)

  • Zhenming Xie

    (Zhejiang University)

  • Binqiang Wang

    (Zhejiang University)

  • Rui Ye

    (Zhejiang University)

  • Xinwen Ou

    (Zhejiang University)

  • Chen Wang

    (Zhejiang University)

  • Ning Yu

    (Zhejiang University)

  • Cheng Huang

    (Zhejiang University)

  • Jie Zhao

    (Zhejiang University)

  • Chunhui Cai

    (Zhejiang University)

  • Furong Zhang

    (Zhejiang University)

  • Damiano Buratto

    (Zhejiang University
    Zhejiang University)

  • Taimoor Khan

    (Zhejiang University
    Zhejiang University)

  • Yan Qiao

    (Chinese Academy of Sciences)

  • Yuejin Hua

    (Zhejiang University
    Ningbo University
    Zhejiang University)

  • Ruhong Zhou

    (Zhejiang University
    Shanghai Institute for Advanced Study of Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Bing Tian

    (Zhejiang University
    Zhejiang University)

Abstract

Protocell fitness under extreme prebiotic conditions is critical in understanding the origin of life. However, little is known about protocell’s survival and fitness under prebiotic radiations. Here we present a radioresistant protocell model based on assembly of two types of coacervate droplets, which are formed through interactions of inorganic polyphosphate (polyP) with divalent metal cation and cationic tripeptide, respectively. Among the coacervate droplets, only the polyP-Mn droplet is radiotolerant and provides strong protection for recruited proteins. The radiosensitive polyP-tripeptide droplet sequestered with both proteins and DNA could be encapsulated inside the polyP-Mn droplet, and form into a compartmentalized protocell. The protocell protects the inner nucleoid-like condensate through efficient reactive oxygen species’ scavenging capacity of intracellular nonenzymic antioxidants including Mn-phosphate and Mn-peptide. Our results demonstrate a radioresistant protocell model with redox reaction system in response to ionizing radiation, which might enable the protocell fitness to prebiotic radiation on the primitive Earth preceding the emergence of enzyme-based fitness. This protocell might also provide applications in synthetic biology as bioreactor or drug delivery system.

Suggested Citation

  • Shang Dai & Zhenming Xie & Binqiang Wang & Rui Ye & Xinwen Ou & Chen Wang & Ning Yu & Cheng Huang & Jie Zhao & Chunhui Cai & Furong Zhang & Damiano Buratto & Taimoor Khan & Yan Qiao & Yuejin Hua & Ruh, 2023. "An inorganic mineral-based protocell with prebiotic radiation fitness," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43272-5
    DOI: 10.1038/s41467-023-43272-5
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    References listed on IDEAS

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    1. Sheref S. Mansy & Jason P. Schrum & Mathangi Krishnamurthy & Sylvia Tobé & Douglas A. Treco & Jack W. Szostak, 2008. "Template-directed synthesis of a genetic polymer in a model protocell," Nature, Nature, vol. 454(7200), pages 122-125, July.
    2. Can Xu & Nicolas Martin & Mei Li & Stephen Mann, 2022. "Living material assembly of bacteriogenic protocells," Nature, Nature, vol. 609(7929), pages 1029-1037, September.
    3. Siddharth Deshpande & Frank Brandenburg & Anson Lau & Mart G. F. Last & Willem Kasper Spoelstra & Louis Reese & Sreekar Wunnava & Marileen Dogterom & Cees Dekker, 2019. "Spatiotemporal control of coacervate formation within liposomes," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    4. Bernardo Gouveia & Yoonji Kim & Joshua W. Shaevitz & Sabine Petry & Howard A. Stone & Clifford P. Brangwynne, 2022. "Capillary forces generated by biomolecular condensates," Nature, Nature, vol. 609(7926), pages 255-264, September.
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