Chiral and nematic phases of flexible active filaments

Abstract

The emergence of large-scale order in self-organized systems relies on local interactions between individual components. During bacterial cell division, the tubulin-homolog FtsZ polymerizes into treadmilling filaments that further assemble into a cytoskeletal ring. Although minimal in vitro assays have shown the striking self-organization capacity of FtsZ filaments, such as dynamic chiral assemblies, how these large-scale structures emerge and relate to individual filament properties remains poorly understood. To understand this quantitatively, we combined minimal chiral active matter simulations with biochemical reconstitution experiments. Using STED and TIRF microscopy as well as high-speed AFM, we imaged the behavior of FtsZ filaments on different spatial scales. Simulations and experiments revealed that filament density and flexibility define the local and global order of the system: At intermediate densities, flexible filaments organize into chiral rings and polar bands, while an effectively nematic organization dominates for high filament densities and for mutant filaments with increased rigidity. Our predicted phase diagram captured these features quantitatively, demonstrating how filament flexibility, density and chirality cooperate with activity to give rise to a large repertoire of collective behaviors. These properties are likely important for the dynamic organization of soft chiral matter, including that of treadmilling FtsZ filaments during bacterial cell division.

Self-organisation of mortal filaments: the role of FtsZ treadmilling in bacterial division ring formation

“…Strikingly, Figure 2b demonstrates that both HS-AFM and simulation trajectories display the same coupling between orientational order and density, independently of the specific kinetic parameters used. Furthermore, when we perform HS-AFM with an FtsZ mutant with reduced GTPase activity and greatly inhibited depolymerisation (FtsZ L169R) [9], we observe that, just like in simulations, nematic defects are not resolved over time and the system remains at lower nematic order than wild type (Figure 2d and Supplementary Movie 6). These results indicate that the our modelling approach accurately describes FtsZ treadmilling behaviour as observed experimentally and should therefore provide insight into the mechanisms underlying the filament ordering.…”

“…From a physics point of view, treadmilling has been often modelled as self-propulsion, where the filament centre of mass moves directionally with a certain velocity to mimic the directional filament growth [7][8][9]. While this approach might be appropriate to describe single filament dynamics, when it comes to the assembly into higher order dynamic structures, self-propelled models might not be suitable.…”

Nanoscopic Elucidation of Spontaneous Self-Assembly of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Open Reading Frame 6 (ORF6) Protein

“…HS-AFM solves the technical limitations of cryoelectron microscopy (cryo-EM) and X-ray crystallography for investigating the structural properties of proteins with intrinsically disordered regions (IDRs) . Moreover, the temporal resolution of HS-AFM supersedes other imaging tools in capturing the structural dynamics of biomolecules, − the dynamics of biomolecule interactions, − and the dynamics of biomolecule–organelle interactions. − Here, we use HS-AFM to elucidate the full-length ORF6 protein structure and its intrinsic molecular dynamics. ORF6 appeared as oligomers, and these oligomers readily formed short or long protofilaments, especially at higher temperatures or on fluidic lipid surfaces.…”