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.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Code availability
Mathematica (version 11.3.0.0) custom algorithms were developed and used to analyse the theoretical model in Fig. 3 and Supplementary Note 4. Matlab (R2017b) custom algorithms were developed and used to compute sliding displacements from strip curvature (Fig. 1e and Supplementary Note 1) and to implement the computational model in Fig. 4 and Supplementary Note 5. These computer codes are available from the corresponding authors upon reasonable request.
Data availability
The data that support the plots within this paper and other findings of this study are available from the corresponding authors upon request.
References
Buetow, D. E. The Biology of Euglena: Physiology (Academic Press, New York, 1982).
Leander, B. S. Euglenida: euglenids or euglenoids. v.10 http://tolweb.org/Euglenida/97461/2012.11.10 (November 2012, The Tree of Life Web project).
Leander, B. S., Lax, G., Karnkowska, A. & Simpson, A. G. B. in Handbook of the Protists (eds Archibald, J. et al.) Ch. 29 (Springer, Cham, 2017).
Dobell, C. Antony van Leeuwenhoek and his ‘Little Animals’ (Dover, New York, 1932).
Suzaki, T. & Williamson, R. E. Euglenoid movement in Euglena fusca: evidence for sliding between pellicular strips. Protoplasma 124, 137–146 (1985).
Suzaki, T. & Williamson, R. E. Reactivation of the euglenoid movement and flagellar beating in detergent-extracted cells of Astasia longa: different mechanisms of force generation are involved. J. Cell Sci. 80, 75–89 (1986).
Arroyo, M., Heltai, L., Millán, D. & DeSimone, A. Reverse engineering the euglenoid movement. Proc. Natl Acad. Sci. USA 109, 17874–17879 (2012).
Fletcher, D. A. & Theriot, J. A. An introduction to cell motility for the physical scientist. Phys. Biol. 1, T1–T10 (2004).
Avron, J. E., Kenneth, O. & Oaknin, D. H. Pushmepullyou: an efficient micro-swimmer. New J. Phys. 7, 234 (2005).
Rossi, M., Cicconofri, G., Beran, A., Noselli, G. & DeSimone, A. Kinematics of flagellar swimming in Euglena gracilis: helical trajectories and flagellar shapes. Proc. Natl Acad. Sci. USA 114, 13085–13090 (2017).
Yamaguchi, A., Yubuki, N. & Leander, B. S. Morphostasis in a novel eukaryote illuminates the evolutionary transition from phagotrophy to phototrophy: description of Rapaza viridis n. gen. et sp. (Euglenozoa, Euglenida). BMC Evol. Biol. 12, 29 (2012).
Leander, B. S., Esson, H. J. & Breglia, S. A. Macroevolution of complex cytoskeletal systems in euglenids. Bioessays 29, 987–1000 (2007).
Karnkowska, A. et al. Phylogenetic relationships and morphological character evolution of photosynthetic euglenids (Excavata) inferred from taxon-rich analyses of five genes. J. Eukaryot. Microbiol. 62, 362–373 (2015).
Esson, H. J. & Leander, B. S. Novel pellicle surface patterns on Euglena obtusa (euglenophyta) from the marine benthic environment: implications for pellicle development and evolution. J. Phycol. 44, 132–141 (2008).
Jennings, H. S. Contributions to the Study of the Behaviour of Lower Organisms (Carnegie Institution of Washington, Washington, D.C., 1904).
Suzaki, T. & Williamson, R. E. Cell surface displacement during euglenoid movement and its computer simulation. Cell Motil. Cytoskel. 6, 186–192 (1986).
Lin, J. & Nicastro, D. Asymmetric distribution and spatial switching of dynein activity generates ciliary motility. Science 360, eaar1968 (2018).
Arroyo, M. & DeSimone, A. Shape control of active surfaces inspired by the movement of euglenids. J. Mech. Phys. Solids. 62, 99–112 (2014).
Milo, R. & Phillips, R. Cell Biology by the Numbers (Garland Science, New York, 2015).
Purcell, E. M. Life at low Reynolds numbers. Am. J. Phys. 45, 3–11 (1977).
Wu, H. et al. Amoeboid swimming in a channel. Soft Matter 12, 7470–7484 (2016).
Hawkins, R. J. et al. Pushing off the walls: a mechanism of cell motility in confinement. Phys. Rev. Lett. 102, 058103 (2009).
Hawkins, R. J. et al. Spontaneous contractility-mediated cortical flow generates cell migration in three-dimensional environments. Biophys. J. 101, 1041–1045 (2011).
Bergert, M. et al. Force transmission during adhesion-independent migration. Nat. Cell Biol. 17, 524–529 (2015).
Prentice-Mott, H. V. et al. Biased migration of confined neutrophil-like cells in asymmetric hydraulic environments. Proc. Natl Acad. Sci. USA 110, 21006–21011 (2013).
Liu, Y. J. et al. Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells. Cell 160, 659–672 (2015).
Moreau, H. D. et al. Macropinocytosis overcomes directional bias due to hydraulic resistance to enhance space exploration by dendritic cells. Preprint at https://doi.org/10.1101/272682 (2018).
Lighthill, M. J. On the squirming motion of nearly spherical deformable bodies through liquids at very small Reynolds numbers. Commun. Pure Appl. Math. 5, 109–118 (1952).
Murray, J. M. Control of cell shape by calcium in the Euglenophyceae. J. Cell Sci. 49, 99–117 (1981).
Svoboda, K. & Block, S. M. Force and velocity measured for single kinesin molecules. Cell 77, 773–784 (1994).
Abraham, Z., Hawley, E., Hayosh, D., Webster-Wood, V. A. & Akkus, O. Kinesin and dynein mechanics: measurement methods and research applications. J. Biomech. Eng. 140, 020805 (2018).
Fritz-Laylin, L. K. et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631–642 (2010).
Pfeifer, R., Lungarella, M. & Iida, F. Self-organization, embodiment, and biologically inspired robotics. Science 318, 1088–1093 (2007).
Kim, S., Laschi, C. & Trimmer, B. Soft robotics, a bio-inspired evolution in robotics. Trends Biotechnol. 31, 287–294 (2013).
Sbalzarini, I. & Koumoutsakos, P. Feature point tracking and trajectory analysis for video imaging in cell biology. J. Struct. Biol. 151, 182–195 (2005).
Acknowledgements
G.N. and A.D.S. acknowledge the support of the European Research Council (AdG-340685-MicroMotility). M.A. acknowledges the support of the European Research Council (CoG-681434), the Generalitat de Catalunya (2017-SGR-1278 and ICREA Academia prize for excellence in research). We thank S. Guido for helpful discussions in the early stages of this study.
Author information
Authors and Affiliations
Contributions
G.N., M.A. and A.D.S. conceived the study. A.B. provided cells and culture expertise. G.N. performed the experiments. G.N., M.A. and A.D.S. analysed the data, performed theoretical analysis and wrote the paper.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Journal peer review information: Nature Physics thanks Andrew Callan-Jones and other anonymous reviewer(s) for their contribution to the peer review of this work.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary Notes 1–6, Supplementary Figures 1–5 and Supplementary References 36–42.
Supplementary Video 1
Video recordings of Euglena gracilis between glass slides separated by a spacer of thickness ∼80 µm. In dilute cultures (left), cells exhibit flagellar swimming without cell shape changes. In crowded cultures (right), cells display a variety of behaviours, including flagellar swimming, cell rounding and spinning, and large-amplitude periodic cell body deformations typical of metaboly.
Supplementary Video 2
Euglena gracilis cells exhibiting metaboly and directed motion in the anterior-to-posterior direction while confined between glass slides. Observation using bright-field reflected light microscopy reveals the reconfigurations of the striated cell envelope concomitant with cell body deformations in the plane of the glass slide. The separation between the slides is ∼6 µm.
Supplementary Video 3
Euglena gracilis cells exhibiting metaboly and directed motion in the anterior-to-posterior direction while confined between glass slides. Observation using bright-field reflected light microscopy reveals the reconfigurations of the striated cell envelope concomitant with cell body deformations in the plane of the glass slide. The separation between the slides is ∼4 µm.
Supplementary Video 4
Video recordings of Euglena gracilis in tapered capillaries. Cells swimming into tapered capillaries transition from flagellar swimming (top left) to developing large-amplitude shape excursions (top right), including rounding (bottom left). When confined in capillary diameters smaller than about twice the free-swimming cell diameter, most cells develop the prototypical peristaltic cell body deformations of metaboly (bottom right).
Supplementary Video 5
Euglena gracilis cell confined in a glass capillary and imaged using bright-field reflected light microscopy. Rounding of the cell body, as determined by the reconfigurations of the pellicle strips, allows the cell to switch its orientation. The microscope was intermittently focused at the pellicle/capillary interface to visualize the pellicle and at the capillary axis to visualize cell shape.
Supplementary Video 6
Video recordings of Euglena gracilis exhibiting metaboly and directed motion in tapered capillaries under increasing confinement, as quantified by the ratio of dcap/dcell, along with kymographs relative to the capillary axis. The movie shows that crawling by metaboly is effective up to very large degree of confinement.
Supplementary Video 7
Video recordings of Euglena gracilis not exhibiting body deformations and acting as hydraulic plugs driven by a known pressure difference, pin, of increasing magnitude between the capillary extremities. Data from these experiments allowed us to quantify a viscous and confinement-dependent friction between cells and the capillary walls.
Supplementary Video 8
Video recordings of Euglena cells stuck in a glass capillary and beating their anterior flagellum.
Supplementary Video 9
Results from the idealized model for the power phase of metaboly in the limit of infinite wall friction relative to hydraulic resistance (top), in the limit of zero wall friction relative to hydraulic resistance (bottom), and for an intermediate case where hydraulic propulsive forces and frictional resistive forces compete (middle). The blue arrows report the average fluid velocity induced by the cell, defined as the flow rate divided by the cross-sectional area of the capillary. The surface of the idealized model is decorated along slip lines by material particles to highlight their motion relative to the capillary walls in the contact region.
Supplementary Video 10
Video recordings of an Euglena cell effectively crawling by metaboly (right) in the presence of an immobile cell, stuck in the capillary and acting as a hydraulic plug (left).
Supplementary Video 11
Video recordings of Euglena gracilis performing metaboly in a capillary and of suspended polystyrene beads by combining bright-field and fluorescence microscopy. Data from these experiments allowed us to quantify the fluid flow around crawling cells by tracking the fluorescent beads. Only beads in the vicinity of the cell undergo rapid motions due to local flows induced by shape changes and flagellar beating.
Supplementary Video 12
Euglena gracilis crawling by metaboly while confined into a glass capillary. Observation using bright-field reflected light microscopy allows for the visualization of the pellicle strips in contact with the capillary wall. The microscope was intermittently focused at the pellicle/capillary interface to visualize the pellicle and at the capillary axis to visualize cell shape. The movie also reports the kymograph relative to the capillary axis. The trajectories of pellicle features reveal sliding between the pellicle and the capillary wall in the contact region.
Supplementary Video 13
Computational results from the theoretical model of crawling by metaboly under confinement. Results are shown for increasing confinement, as quantified by the ratio of dcap/dcell = {0.875, 1.0, 1.375, 1.8}, in the limit of high hydraulic resistance, and during three cycles. The cell motion is reported by black and white features fixed in the frame of the capillary. Notice that the model self-adapts to imposed confinement by developing a limit cycle (gait), which is consistent with the experimental observations on Euglena cells. The four gaits at different degrees of confinement are the result on the same activation pattern, represented as a space–time colour map (left).
Supplementary Video 14
Video recordings of Distigma proteus between glass slides separated on one side by a spacer of thickness ∼80 µm in order to realize a wedge-shaped fluid chamber. In the absence of confinement (gap between plates ∼36 µm), cells exhibit flagellar swimming. Significant confinement between the two plates (gap ∼5 µm) triggers non-reciprocal peristaltic cell deformations, which allow Distigma cells to crawl.
Supplementary Video 15
Video recordings of Peranema trichophorum between glass slides separated on one side by a spacer of thickness ∼80 µm in order to realize a wedge-shaped fluid chamber. In the absence of confinement (gap between plates ∼52–43 µm), cells glide on the substrate thanks to the movement of their flagellum. During gliding, cells occasionally bend their body, and this shape change is associated with sharp turns of the cell trajectory. Under high confinement between the glass plates (gap ∼7 µm), cells are not able to glide and develop periodic, largely reciprocal shape changes.
Rights and permissions
About this article
Cite this article
Noselli, G., Beran, A., Arroyo, M. et al. Swimming Euglena respond to confinement with a behavioural change enabling effective crawling. Nat. Phys. 15, 496–502 (2019). https://doi.org/10.1038/s41567-019-0425-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41567-019-0425-8
This article is cited by
-
Light-controlled soft bio-microrobot
Light: Science & Applications (2024)
-
Coated microbubbles swim via shell buckling
Communications Engineering (2023)
-
Large-Scale Dynamics of Self-propelled Particles Moving Through Obstacles: Model Derivation and Pattern Formation
Bulletin of Mathematical Biology (2020)