Material properties of biomolecular condensates emerge from nanoscale dynamics.

Abstract

Biomolecular condensates form by phase separation of biological polymers and have important functions in the cell $-$ functions that are inherently connected to their physical properties. A remarkable aspect of such condensates is that their viscoelastic properties can vary by orders of magnitude, but it has remained unclear how these pronounced differences are rooted in the nanoscale dynamics at the molecular level. Here we investigate a series of condensates formed by complex coacervation that span about two orders of magnitude in molecular dynamics, diffusivity, and viscosity. We find that the nanoscale chain dynamics on the nano- to microsecond timescale can be accurately related to both translational diffusion and mesoscale condensate viscosity by analytical relations from polymer physics. Atomistic simulations reveal that the observed differences in friction $-$ a key quantity underlying these relations $-$ are caused by differences in inter-residue contact lifetimes, leading to the vastly different dynamics among the condensates. The rapid exchange of inter-residue contacts we observe may be a general mechanism for preventing dynamic arrest in compartments densely packed with polyelectrolytes, such as the cell nucleus.