Non-associative phase separation in an evaporating droplet as a model for prebiotic compartmentalization

Wei Guo, Andrew B. Kinghorn, Yage Zhang, Qingchuan Li, Aditi Dey Poonam, Julian A. Tanner () and Ho Cheung Shum ()
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Wei Guo: The University of Hong Kong, Hong Kong (SAR)
Andrew B. Kinghorn: School of Biomedical Sciences, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong (SAR)
Yage Zhang: The University of Hong Kong, Hong Kong (SAR)
Qingchuan Li: The University of Hong Kong, Hong Kong (SAR)
Aditi Dey Poonam: The University of Hong Kong, Hong Kong (SAR)
Julian A. Tanner: School of Biomedical Sciences, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong (SAR)
Ho Cheung Shum: The University of Hong Kong, Hong Kong (SAR)

Nature Communications, 2021, vol. 12, issue 1, 1-13

Abstract: Abstract The synthetic pathways of life’s building blocks are envisaged to be through a series of complex prebiotic reactions and processes. However, the strategy to compartmentalize and concentrate biopolymers under prebiotic conditions remains elusive. Liquid-liquid phase separation is a mechanism by which membraneless organelles form inside cells, and has been hypothesized as a potential mechanism for prebiotic compartmentalization. Associative phase separation of oppositely charged species has been shown to partition RNA, but the strongly negative charge exhibited by RNA suggests that RNA-polycation interactions could inhibit RNA folding and its functioning inside the coacervates. Here, we present a prebiotically plausible pathway for non-associative phase separation within an evaporating all-aqueous sessile droplet. We quantitatively investigate the kinetic pathway of phase separation triggered by the non-uniform evaporation rate, together with the Marangoni flow-driven hydrodynamics inside the sessile droplet. With the ability to undergo liquid-liquid phase separation, the drying droplets provide a robust mechanism for formation of prebiotic membraneless compartments, as demonstrated by localization and storage of nucleic acids, in vitro transcription, as well as a three-fold enhancement of ribozyme activity. The compartmentalization mechanism illustrated in this model system is feasible on wet organophilic silica-rich surfaces during early molecular evolution.

Date: 2021
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DOI: 10.1038/s41467-021-23410-7

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