Swimming Euglena respond to confinement with a behavioural change enabling effective crawling

TL;DR

Euglena cells switch from flagellar swimming to a robust crawling mode in confined environments, driven by mechanical self-regulation rather than mechanosensitive feedback, enabling effective locomotion under extreme confinement.

Contribution

This study reveals that Euglena's peristaltic deformation functions as an adaptive crawling mechanism triggered by confinement, supported by a computational model explaining its self-regulation.

Findings

Confinement triggers a switch from flagellar swimming to crawling.

Euglena can navigate extreme geometric confinement effectively.

Gait adaptability arises from mechanical self-regulation, not mechanosensitive feedback.

Abstract

Some euglenids, a family of aquatic unicellular organisms, can develop highly concerted, large-amplitude peristaltic body deformations. This remarkable behaviour 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 behaviour 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 modelling 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.