Controlling Forces and Organization in Active Matter

An engineered system of molecular motors and filaments is controlled with light to form structures and force fields on the mesoscopic length scale.

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An immune cell meandering along a blood vessel catches the scent of an intruder, a bacteria, and rapidly crawls towards it. After making several sharp turns and ploughing past some innocent blood cells, it finally reaches the bacteria and engulfs it. Within the immune cell, the confined bacteria is carried to an acidic bath where it meets its doom. 

The immune cell chases down the bacteria by controlling dynamic structures and forces within the cell. This precise microscopic control is unmatched by our current technological capabilities, and the underlying principles are largely unknown. Under the hood, cells perform these feats by using molecules that are constantly burning chemical fuel to generate forces and move. These self-propelled, or "active" molecules make up all living things. They are the engines that allow organisms to move through and modify their environments. In fact, the fundamental act of replication occurs through the collective behavior of active molecules to form  "spindle" structures that pull packaged DNA into new daughter cells. 

Here is one of the key challenges to engineering with active matter: while it has been shown that mixtures of these molecules in a test tube can spontaneously organize into various structures and generate forces, there has so far been no way to control when and where these activities occur. If we are to eventually build cell-like machines that can organize molecular cargo or hunt down cancer cells, we need to be able to control systems of active molecules.

In this work, we engineer a system of active molecules so that they can be controlled to organize structures and forces with light. Our system consists of three primary components: biomolecular motors, polar filaments, and a chemical fuel. A molecular motor burns chemical fuel as it runs across a filament. The polarization of the filaments means that the motors always run towards one end, the “plus” end. This mixture alone doesn't do much, motors consume fuel as they zip all over but the filaments float around indifferently. Things are different, however,  when motors form pairs.

When the motors are paired up, they pull on each other as they run along neighboring filaments. These pulling forces are transmitted to the filaments, causing them to move. Since the motors are all running towards the filament plus ends, filaments become organized so that all of the plus ends are brought together to form an "aster" structure. We control motor pairing with light such that an aster forms within a lit region, and outside this region the filaments remain disordered.

In some ways, the light is acting as a source of information. We use the light to toggle between different interaction rules between motors, allowing us to choose when and where these filaments are reorganized. By shining patterns of light into the mixture, we can generate asters of different sizes, move them along arbitrary paths, and even merge them together. In addition, we find that the reorganization of many filaments results in the generation of fluid flows, which are notoriously hard to generate on this small length-scale (see microfluidics).

In spite of the few components that our system entails, the variety of phenomena we see opens many questions. For example, how speeds are amplified beyond the run speed of a single motor, and what limits this amplification effect. Our system then, not only provides a test bed for engineering further control, but also a rich resource to develop theories of active matter and biophysics. While there is still a lot of catching up to do to reach the exquisite  control a cell has over active matter, we hope this work will open a new frontier in active matter physics and engineering.

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Tyler Ross

PhD Student, Caltech

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