Encapsulated bacteria deform lipid vesicles into flagellated swimmers

We study a synthetic system of motile Escherichia coli bacteria encapsulated inside giant lipid vesicles. Forces exerted by the bacteria on the inner side of the membrane are sufficient to extrude membrane tubes filled with one or several bacteria. We show that a physical coupling between the membrane tube and the flagella of the enclosed cells transforms the tube into an effective helical flagellum propelling the vesicle. We develop a simple theoretical model to estimate the propulsive force from the speed of the vesicles and demonstrate the good efficiency of this coupling mechanism. Together, these results point to design principles for conferring motility to synthetic cells.

The interaction of active and passive matter lies at the heart of biology. Active matter (1) consists of collections of entities that consume energy from their environment to generate mechanical forces, which often result in motion. Thus, the cell membrane, whose essential component is a passive lipid bilayer, can actively remodel during cell growth; motility; and, ultimately, cell evolution, under the forces exerted by a host of active agents. For example, continuous polymerization–depolymerization of actin in the cytoskeleton deforms the eukaryotic cell membrane into two- and one-dimensional protrusions (lamellipodia and filopodia) that can move the whole cell (2, 3). Similar actin-supported membrane protrusions are thought to have facilitated the accidental engulfment of bacteria that led to the emergence of eukaryotic cells (4). The biophysics of active membranes has therefore been subjected to interdisciplinary scrutiny (5). More recently, learning how to create active membranes systems that deform, divide, and propel has become a priority area in the drive to synthesize life ab initio (6).Lipid vesicles enclosing natural or artificial microswimmers are becoming a model system for studying active membranes in vitro (7–15). Such composites have also direct biological relevance. For instance, from inside their eukaryotic hosts, bacterial pathogens such as Rickettsia rickettsii or Listeria monocytogenes (16, 17) continue their life cycles by hijacking the actin polymerization–depolymerization apparatus of their hosts and pushing out a tube-like protuberance from the plasma membrane. The pathogens then contact other host cells or escape into the surrounding medium by means of these membrane tubes (18).To date, research in coupling swimmers with membranes has mostly been theoretical and numerical. Such models have predicted a range of interfacial morphological changes and, in some cases, net motion of the interface (7–13). The experimental realization of these systems was only recently achieved by encapsulating swimming Bacillus subtilis bacteria (14) and synthetic Janus particles (15) in giant lipid vesicles. Both experiments reported nonequilibrium membrane fluctuations and vesicle deformations, ranging from tubular protrusions to dendritic shapes. However, net motion of the vesicles was not observed in either case.Here we present a similar experimental design but with markedly different outcome. Escherichia coli, another common motile bacterium, also extrudes membrane tubes but in addition sets the whole vesicle into motion. We demonstrate that such motion is due to a physical coupling between the flagella bundle of the enclosed cells and the tubes. The tube–flagella composite functions as a helical propeller for the entire vesicle.In biology, the specificity of interactions between bacteria and the membranes of eukaryotic hosts underlies the plethora of parasitic and symbiotic relations that have emerged between cells (18–20). Likewise, our observations illustrate the importance of small details in the design of active matter systems (21). Encapsulated bacteria propelled by a single bundle of helical flagella can generate net motion of the vesicles, whereas encapsulated swimmers propelled at similar speeds by phoresis fail to do so (15). These observations illustrate the fact that it is dangerous to proceed from coarse-grained simulations or theory that neglect such details to predict the behavior of particular systems. At the same time, our results point to a design principle for conferring motility to artificial cell models.