An inorganic mineral-based protocell with prebiotic radiation fitness

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 (), Ruhong Zhou () and Bing Tian ()
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Shang Dai: 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
Taimoor Khan: Zhejiang University
Yan Qiao: Chinese Academy of Sciences
Yuejin Hua: Zhejiang University
Ruhong Zhou: Zhejiang University
Bing Tian: Zhejiang University

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-43272-5

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