A diffusiophoretic mechanism for ATP-driven transport without motor proteins

Beatrice Ramm,Kristina A Ganzinger,Philipp Blumhardt,Alena Khmelinskaia,Hiromune Eto,Petra Schwille,Andriy Goychuk,Erwin Frey

doi:10.1038/s41567-021-01213-3

Abstract

The healthy growth and maintenance of a biological system depends on the precise spatial organization of molecules within the cell through the dissipation of energy. Reaction–diffusion mechanisms can facilitate this organization, as can directional cargo transport orchestrated by motor proteins, by relying on specific protein interactions. However, transport of material through the cell can also be achieved by active processes based on non-specific, purely physical mechanisms, a phenomenon that remains poorly explored. Here, using a combined experimental and theoretical approach, we discover and describe a hidden function of the Escherichia coli MinDE protein system: in addition to forming dynamic patterns, this system accomplishes the directional active transport of functionally unrelated cargo on membranes. Remarkably, this mechanism enables the sorting of diffusive objects according to their effective size, as evidenced using modular DNA origami–streptavidin nanostructures. We show that the diffusive fluxes of MinDE and non-specific cargo couple via density-dependent friction. This non-specific process constitutes a diffusiophoretic mechanism, as yet unknown in a cell biology setting. This nonlinear coupling between diffusive fluxes could represent a generic physical mechanism for establishing intracellular organization.

Highlights

Spatiotemporal organization of cells generally emerges through redistribution and transport of molecules via motor proteins[1], self-assembling cytoskeletal elements[2] or self-organizing reaction–diffusion systems[3]
NTPases that drive the transport is usually mediated by specific protein–protein interactions
Non-specific coupling of biomolecules, by contrast, is poorly explored in biology and, so far, only a few examples of molecular transport based on purely physical mechanisms have been reported

Summary

Introduction

Spatiotemporal organization of cells generally emerges through redistribution and transport of molecules via motor proteins[1], self-assembling cytoskeletal elements[2] or self-organizing reaction–diffusion systems[3]. We discerned how the effective size (that is, membrane footprint) and diffusion coefficient of the cargo, as well as the type of MinDE patterns, determine the transport that takes place.

Results

Conclusion