Energy landscapes and heat capacity signatures for peptides correlate with phase separation propensity

Author:

Nicy ORCID,Joseph Jerelle AORCID,Collepardo-Guevara RosanaORCID,Wales David J.ORCID

Abstract

Phase separation plays an important role in the formation of membraneless compartments within the cell, and intrinsically disordered proteins with low-complexity sequences can drive this compartmentalisation. Various intermolecular forces, such as aromatic–aromatic and cation–aromatic interactions, promote phase separation. However, little is known about how the ability of proteins to phase separate under physiological conditions is encoded in their energy landscapes, and this is the focus of the present investigation. Our results provide a first glimpse into how the energy landscapes of minimal peptides that containππand cation–πinteractions differ from the peptides that lack amino acids with such interactions. The peaks in the heat capacity (CV) as a function of temperature report on alternative low-lying conformations that differ significantly in terms of their enthalpic and entropic contributions. The CVanalysis and subsequent quantification of frustration of the energy landscape suggest that the interactions that promote phase separation leads to features (peaks or inflection points) at low temperatures in CV, more features may occur for peptides containing residues with better phase separation propensity and the energy landscape is more frustrated for such peptides. Overall, this work links the features in the underlying single-molecule potential energy landscapes to their collective phase separation behaviour, and identifies quantities (CVand frustration metric) that can be utilised in soft material design.

Publisher

Cold Spring Harbor Laboratory

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