Euglenoid movement inEuglena fusca: Evidence for sliding between pellicular strips

Suzaki, Toshinobu; Williamson, R. E.

doi:10.1007/bf01279733

Cited by 63 publications

(49 citation statements)

References 18 publications

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“…S3C). This observation is consistent with the hypothesis that pellicle deformation is mediated by relative sliding of pellicle strips, which retain their length and width (9). Such a deformation is called simple shear in continuum mechanics, and preserves area locally.…”

supporting

confidence: 89%

Reverse engineering the euglenoid movement

Arroyo

Heltai

Millán

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

103

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Euglenids exhibit an unconventional motility strategy amongst unicellular eukaryotes, consisting of large-amplitude highly concerted deformations of the entire body (euglenoid movement or metaboly). A plastic cell envelope called pellicle mediates these deformations. Unlike ciliary or flagellar motility, the biophysics of this mode is not well understood, including its efficiency and molecular machinery. We quantitatively examine video recordings of four euglenids executing such motions with statistical learning methods. This analysis reveals strokes of high uniformity in shape and pace. We then interpret the observations in the light of a theory for the pellicle kinematics, providing a precise understanding of the link between local actuation by pellicle shear and shape control. We systematically understand common observations, such as the helical conformations of the pellicle, and identify previously unnoticed features of metaboly. While two of our euglenids execute their stroke at constant body volume, the other two exhibit deviations of about 20% from their average volume, challenging current models of low Reynolds number locomotion. We find that the active pellicle shear deformations causing shape changes can reach 340%, and estimate the velocity of the molecular motors. Moreover, we find that metaboly accomplishes locomotion at hydrodynamic efficiencies comparable to those of ciliates and flagellates. Our results suggest new quantitative experiments, provide insight into the evolutionary history of euglenids, and suggest that the pellicle may serve as a model for engineered active surfaces with applications in microfluidics.microswimmers | self-propulsion | stroke kinematics | active soft matter U nicellular microorganisms have developed effective ways of locomotion in a fluid, overcoming fundamental physical constraints such as the time reversibility of low Reynolds number (Re) hydrodynamics (1). Amongst eukaryotes, most species swim beating cilia or flagella. Yet, through a long evolutionary history, some protists have developed unconventional functional strategies, accomplished by highly diverse subcellular structures (2). A notable example is the euglenoid movement, or metaboly, executed by some species of euglenids (3). This peculiar motility mode is characterized by elegantly concerted, large-amplitude distortions of the entire cell with frequencies of about f ≈ 0.1 Hz (4). Euglenids have attracted the attention of scientists since the earliest days of microscopy, when van Leeuwenhoek referred to them in 1674 as microscopic motile "animalcules" that were green in the middle, which challenged the classification of organisms into animals and plants (5). More recently, metaboly has inspired models for artificial microswimmers (6), although even its locomotory function remains unclear. In contrast with flagellar or ciliary motion, the euglenoid movement has not undergone close biophysical scrutiny, and fundamental questions remain open, including a precise understanding of the actuation mechanism leading...

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supporting

confidence: 89%

Reverse engineering the euglenoid movement

Arroyo

Heltai

Millán

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

103

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“…Normal Euglena cells change their shape by a process involving the pellicle, a structure composed of parallel strands found in the exterior surface. Detailed analysis of the pellicle of Euglena fusca [Suzaki and Williamson, 1985] showed that these parallel strands slid past each other during changes in body shape. The sliding motion of these strips is consistent with the generation of a torque-like force suggested by particle movement in stratified cells.…”

Section: Discussionmentioning

confidence: 99%

The molecular biology of Euglena gracilis. XV. Recovery from centrifugation‐induced stratification

Kempner¹,

Miller²

2003

Cell Motil. Cytoskeleton

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The contents of Euglena gracilis cells can be separated in vivo by ultracentrifugation. Within the unbroken cell, each set of components forms a distinct layer according to their respective densities. The degree of segregation increases with both the g-force and the time of centrifugation, up to a maximum at 100,000 x g for 1 h, when six distinct strata can be observed. When returned to normal growth conditions, essentially all the cells return to the normal state and growth pattern. Greater g-forces or longer exposures do not alter the observable strata, but the ability of the cells to recover is diminished. Smaller g-forces result in less separation of cellular contents and all cells recover, even after 18 h of exposure. Euglena cells stratified at 100,000 x g for 1 h were returned to normal growth conditions; recovery was followed microscopically and by the rate of utilization of oxygen as well as that of the single carbon source. The cells recovered their normal state within 1 to 2 h, which is only a tenth of the normal doubling time. The mechanism for this recovery involves a natural process of change in cell shape caused by contraction and relaxation of the pellicle, a cell surface structure.

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“…The euglenoid movement is a characteristic motility for the euglenoid flagellates, involving changing the shape of their bodies, which enables the single-cell organisms to swim without waving their flagella2627. The pellicular structures are commonly observed on the surface of the organisms and should be responsible for the movement2829.…”

Section: Discussionmentioning

confidence: 99%

“…The pellicular structures are commonly observed on the surface of the organisms and should be responsible for the movement2829. During the movement, the adjacent pellicular strips slide past each other, maintaining the width and length of the strips2730. In Euglena gracilis , the IP39 proteins are the highly ordered intramembrane particles restricted in the ridge regions of the pellicular membranes1416 and bound to submembrane cytoskeletons1831, and thus may have a stabilizing role for maintaining the strength of the membrane to couple motive forces of the movement with the pellicular sliding.…”

Section: Discussionmentioning

confidence: 99%

The four-transmembrane protein IP39 of Euglena forms strands by a trimeric unit repeat

et al. 2013

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Euglenoid flagellates have striped surface structures comprising pellicles, which allow the cell shape to vary from rigid to flexible during the characteristic movement of the flagellates. In Euglena gracilis, the pellicular strip membranes are covered with paracrystalline arrays of a major integral membrane protein, IP39, a putative four-membrane-spanning protein with the conserved sequence motif of the PMP-22/EMP/MP20/Claudin superfamily. Here we report the three-dimensional structure of Euglena IP39 determined by electron crystallography. Two-dimensional crystals of IP39 appear to form a striated pattern of antiparallel double-rows in which trimeric IP39 units are longitudinally polymerised, resulting in continuously extending zigzag-shaped lines. Structural analysis revealed an asymmetric molecular arrangement in the trimer, and suggested that at least four different interactions between neighbouring protomers are involved. A combination of such multiple interactions would be important for linear strand formation of membrane proteins in a lipid bilayer.

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Euglenoid movement inEuglena fusca: Evidence for sliding between pellicular strips

Cited by 63 publications

References 18 publications

Reverse engineering the euglenoid movement

Reverse engineering the euglenoid movement

The molecular biology of Euglena gracilis. XV. Recovery from centrifugation‐induced stratification

The four-transmembrane protein IP39 of Euglena forms strands by a trimeric unit repeat

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