Polygonal motion and adaptable phototaxis via flagellar beat switching in the microswimmer Euglena gracilis

Abstract

Biological microswimmers exhibit versatile strategies for sensing and navigating their environment [1][2][3][4][5][6][7] , e.g., run-and-tumble 2 and curvature modulation 3 . Here we report a striking behavior of Euglena gracilis, where Euglena cells swim in polygonal trajectories due to exposure to increasing light intensities. While smoothly curved trajectories are common for microswimmers 3,8 , such quantized ones have not been reported previously. This polygonal behavior emerges from periodic switching between the flagellar beating patterns of helical swimming 6, 9 and spinning 10 behaviors. We develop and experimentally validate a biophysical model that describes the phase relationship between the eyespot, cell orientation, light detection, and cellular reorientation, that accounts for all three behavioral states. Coordinated switching between these behaviors allows ballistic, superdiffusive, diffusive, or subdiffusive motion 11,12 (i.e., the tuning of the diffusion constant over 3 orders of magnitude) and enables navigation in structured light fields, e.g., edge avoidance and gradient descent. This feedback-control links multiple system scales (flagellar beats, cellular behaviors, phototaxis strategies) with implications for other natural and synthetic microswimmers 13 .Biological microswimmers exhibit a variety of intricate behaviors and strategies in order to achieve navigational tasks in response to environmental stimuli such as chemicals 1-3 , light 4-6 , electric 1 certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

Control of helical navigation by three-dimensional flagellar beating

“…For algal flagellates, the control of flagellar beating is key to effective spatial navigation and reorientation to photostimuli [11][12][13]. Spermatozoa steer via changes to their 3D beat pattern [14], while ciliates tilt the orientation of ciliary fields to turn [15].…”

Roads to Smart Artificial Microswimmers

“…[78] Phototactic micro-organisms swim and adapt in response to light conditions for optimal photosynthesis. [79,80] Apart from these tactic strategies, natural micro-organisms also respond to other external stimuli such as fluid flows, magnetic field, and gravity and adjust their motility accordingly. [81][82][83] This ability of adapting motions in response to external fields is crucial for effective navigation in biological fluids.…”

The biomechanical role of extra-axonemal structures in shaping the flagellar beat of Euglena

“…the projection on the optic plane) of a beating euglenid flagellum is that of a looping curve, see e.g. [30] for independent observations. Consider now an idealized 3d model of the spinning lasso geometry: a curve with two singular points of concentrated torsion with opposite sign, such as the one shown in Figure 3.…”