A diffusiophoretic mechanism for ATP-driven transport without motor proteins

• Published in: Nature physics 2021-07, Vol.17 (7), p.850-858
• Main Authors: Ramm, Beatrice, Goychuk, Andriy, Khmelinskaia, Alena, Blumhardt, Philipp, Eto, Hiromune, Ganzinger, Kristina A., Frey, Erwin, Schwille, Petra
• Format: Article
• Language: English
• Subjects: 631/57; 639/766/530; 639/766/747; Atomic; Cargo transportation; Cell division; Cell membranes; Classical and Continuum Physics; Complex Systems; Condensed Matter Physics; Coupling (molecular); E coli; Energy dissipation; Fluxes; Friction; Mathematical and Computational Physics; Molecular; Molecular motors; Optical and Plasma Physics; Physics; Physics and Astronomy; Proteins; Theoretical
• ISSN: 1745-2473; 1745-2481
• DOI: 10.1038/s41567-021-01213-3

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. Protein oscillations linked to cell division in Escherichia coli are shown to localize unrelated molecules on the cell membrane via a diffusiophoretic mechanism, in which an effective friction fosters cargo transport along the fluxes set up by the proteins.