Biological condensates form percolated networks with molecular motion properties distinctly different from dilute solutions

Shen, Zeyu1; Jia, Bowen1; Xu, Yang1; Wessen, Jonas2; Pal, Tanmoy2; Chan, Hue Sun2; Du, Shengwang3,4,7; Zhang, Mingjie5,6; Pappu, Rohit, V

2023-06-01

10.7554/eLife.81907

ELIFE   影响因子和分区

2050-084X

Formation of membraneless organelles or biological condensates via phase separation and related processes hugely expands the cellular organelle repertoire. Biological condensates are dense and viscoelastic soft matters instead of canonical dilute solutions. To date, numerous different biological condensates have been discovered, but mechanistic understanding of biological condensates remains scarce. In this study, we developed an adaptive single-molecule imaging method that allows simultaneous tracking of individual molecules and their motion trajectories in both condensed and dilute phases of various biological condensates. The method enables quantitative measurements of concentrations, phase boundary, motion behavior, and speed of molecules in both condensed and dilute phases, as well as the scale and speed of molecular exchanges between the two phases. Notably, molecules in the condensed phase do not undergo uniform Brownian motion, but instead constantly switch between a (class of) confined state(s) and a random diffusion-like motion state. Transient confinement is consistent with strong interactions associated with large molecular networks (i.e., percolation) in the condensed phase. In this way, molecules in biological condensates behave distinctly different from those in dilute solutions. The methods and findings described herein should be generally applicable for deciphering the molecular mechanisms underlying the assembly, dynamics, and consequently functional implications of biological condensates.

phase separation multivalent interaction molecular network formation percolation biological condensate None

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National Natural Science Foundation of China[82188101] ; Minister of Science and Technology of China[2019YFA0508402] ; Shenzhen Bay Laboratory[S201101002] ; Canadian Institutes of Health Research[16104518] ; null[PJT-155930] ; null[RGPIN-2018-04351] ; null[AoE-M09-12] ; null[16101419]

Life Sciences & Biomedicine - Other Topics

Biology

WOS:001009857800001

eLIFE SCIENCES PUBL LTD

Web of Science

1.Hong Kong Univ Sci & Technol, Div Life Sci, Kowloon, ClearWater Bay, Hong Kong, Peoples R China
2.Univ Toronto, Dept Biochem, Toronto, ON, Canada
3.Hong Kong Univ Sci & Technol, Dept Phys, Kowloon, Clear Water Bay, Hong Kong, Peoples R China
4.Hong Kong Univ Sci & Technol, Dept Chem & Biol Engn, Clear Water Bay, Hong Kong, Peoples R China
5.Shenzhen Bay Lab, Greater Bay Biomed Innoctr, Shenzhen, Peoples R China
6.Southern Univ Sci & Technol, Sch Life Sci, Shenzhen, Peoples R China
7.Univ Texas Dallas, Dept Phys, Richardson, TX USA

Shen, Zeyu,Jia, Bowen,Xu, Yang,et al. Biological condensates form percolated networks with molecular motion properties distinctly different from dilute solutions[J]. ELIFE,2023,12.

Shen, Zeyu.,Jia, Bowen.,Xu, Yang.,Wessen, Jonas.,Pal, Tanmoy.,...&Pappu, Rohit, V.(2023).Biological condensates form percolated networks with molecular motion properties distinctly different from dilute solutions.ELIFE,12.

Shen, Zeyu,et al."Biological condensates form percolated networks with molecular motion properties distinctly different from dilute solutions".ELIFE 12(2023).