SignificanceActive flagella provide the propulsion mechanism for a large variety of swimming eukaryotic microorganisms, from protists to sperm cells. Planar and helical beating patterns of these structures are recurrent and widely studied. The fast spinning motion of the locomotory flagellum of the alga Euglena gracilis constitutes a remarkable exception to these patterns. We report a quantitative description of the 3D flagellar beating in swimming E. gracilis. Given their complexity, these shapes cannot be directly imaged with current microscopy techniques. We show how to overcome these limitations by developing a method to reconstruct in full the 3D kinematics of the cell from conventional 2D microscopy images, based on the exact characterization of the helical motion of the cell body.

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Some 250 years after the systematic experiments by Musschenbroek and their rationalization by Euler, for the first time we show that it is possible to design structures (i.e. mechanical systems whose elements are governed by the equation of the elastica) exhibiting bifurcation and instability ('buckling') under tensile load of constant direction and point of application ('dead'). We show both theoretically and experimentally that the behaviour is possible in elementary structures with a single degree of freedom and in more complex mechanical systems, as related to the presence of a structural junction, called 'slider', allowing only relative transversal displacement between the connected elements. In continuous systems where the slider connects two elastic thin rods, bifurcation occurs both in tension and in compression, and is governed by the equation of the elastica, employed here for tensile loading, so that the deformed rods take the form of the capillary curve in a liquid, which is in fact governed by the equation of the elastica under tension. Since axial load in structural elements deeply influences dynamics, our results may provide application to innovative actuators for mechanical wave control; moreover, they open a new perspective in the understanding of failure within structural elements.

Some euglenids, a family of aquatic unicellular organisms, can develop highly concerted, large amplitude peristaltic body deformations. This remarkable behavior has been known for centuries. Yet, its function remains controversial, and is even viewed as a functionless ancestral vestige. Here, by examining swimming Euglena gracilis in environments of controlled crowding and geometry, we show that this behavior is triggered by confinement. Under these conditions, it allows cells to switch from unviable flagellar swimming to a new and highly robust mode of fast crawling, which can deal with extreme geometric confinement and turn both frictional and hydraulic resistance into propulsive forces. To understand how a single cell can control such an adaptable and robust mode of locomotion, we developed a computational model of the motile apparatus of Euglena cells consisting of an active striated cell envelope. Our modeling shows that gait adaptability does not require specific mechanosensitive feedback but instead can be explained by the mechanical self-regulation of an elastic and extended motor system. Our study thus identifies a locomotory function and the operating principles of the adaptable peristaltic body deformation of Euglena cells.

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