Cytomotive actins and tubulins share a polymerisation switch mechanism conferring robust dynamics

Protein filaments are used in myriads of ways to organise other molecules in space and time within cells. Some filament-forming proteins couple the hydrolysis of nucleotides to their polymerisation cycle, thus powering the directed movement of other molecules. These filaments are termed cytomotive. Only members of the actin and tubulin protein superfamilies are known to form cytomotive filaments. We sought to examine the basis of cytomotivity via structural studies of the polymerisation cycles of actin and tubulin homologues from across the tree of life. We analysed published data and performed new structural experiments designed to disentangle functional components of these complex filament systems. In sum, our analysis demonstrates the existence of shared subunit polymerisation switches amongst both cytomotive actins and tubulins, i.e. the conformation of subunits switches upon assembly into filaments. Such cytomotive switches explain filament robustness, by enabling the coupling of kinetic and structural polarities required for useful cytomotive behaviours, and by ensuring that single cytomotive filaments do not fall apart.