B. G. Rodriguez, K. Makasewicz, G. Tesei, F. Eklund, E. Johansson, P. Arosio, G. Volpe, D. S. Midtvedt
Biomolecular condensates can be heterogeneous in composition, morphology, and material properties, but resolving this heterogeneity at the level of individual submicrometer condensates remains challenging. Here, we combine off-axis holographic imaging with quantitative light-scattering analysis and particle tracking to simultaneously measure the size, optical properties, interfacial structure, and hydrodynamic mobility of hundreds of individual condensates per minute. Applied to condensates formed by the N-terminal domain of Ddx4 (Ddx4N1), the method reveals two populations with distinct scattering signatures: compact particles with well-defined interfaces and structurally heterogeneous, non-compact assemblies. Their relative abundance varies systematically with ionic strength. Synthetic polymer controls show that pronounced structural heterogeneity is not a generic consequence of phase separation and suggest a role for interaction heterogeneity in promoting competing mesoscale structures. Mass-size scaling and Brownian aggregation simulations further show that aggregation with incomplete fusion of smaller protein-rich units provides a physical model for the non-compact population. Simultaneous optical and diffusion measurements further show that the two populations have distinct hydrodynamic properties. These results demonstrate that chemically homogeneous condensate-forming systems can populate distinct mesoscale structures that are obscured by ensemble-averaged measurements.