Myosin Lever Arm Directs the Collective Movement Patterns of Motor Proteins

Abstract

The emergence of movement patterns, as in flocking of birds and schooling of fish, is a widespread phenomenon in nature. This collective movement can also be seen at the nanoscale in how the molecular motor myosin teams up to drive muscle contraction, membrane traffic, and cell division in biological cells. To systematically dissect the role of intra- and inter-motor interactions on collective function, we engineered a model system consisting of a branched polarized actin network and a biomimetic DNA origami scaffold patterned with defined number of myosin V and VI. Here, we report on the emergent movement patterns of scaffolds patterned with myosin V and VI. Quantitative analysis of the scaffold movement patterns shows that most myosin VI trajectories are linear while a substantial fraction of myosin V trajectories are highly skewed. We find the flexibile lever arm of myosin VI gives rise to the observed linear movement patterns, while the skewed trajectories of scaffolds with myosin V motors is driven by their rigid lever arm. By pairing simulations and experiments with chimeras, we find that the interplay between the torsional strain on the motor lever arm and inter-motor tension dictates collective motion in groups of motors. Our findings suggest that structural features unique to each myosin confer selective advantages to cellular functions. Beyond the biological relevance, our study uncovers a simple engineering principle for designing efficient molecular transporters.