Literature DB >> 23047705

Reverse engineering the euglenoid movement.

Marino Arroyo1, Luca Heltai, Daniel Millán, Antonio DeSimone.   

Abstract

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.

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Year:  2012        PMID: 23047705      PMCID: PMC3497777          DOI: 10.1073/pnas.1213977109

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  22 in total

1.  A global geometric framework for nonlinear dimensionality reduction.

Authors:  J B Tenenbaum; V de Silva; J C Langford
Journal:  Science       Date:  2000-12-22       Impact factor: 47.728

2.  Propulsion of Microorganisms by Surface Distortions.

Authors: 
Journal:  Phys Rev Lett       Date:  1996-11-04       Impact factor: 9.161

3.  Trends in the evolution of the euglenid pellicle.

Authors:  B S Leander; R P Witek; M A Farmer
Journal:  Evolution       Date:  2001-11-11       Impact factor: 3.694

4.  Optimal feeding and swimming gaits of biflagellated organisms.

Authors:  Daniel Tam; A E Hosoi
Journal:  Proc Natl Acad Sci U S A       Date:  2011-01-03       Impact factor: 11.205

5.  Applied physics. The material is the machine.

Authors:  Kaushik Bhattacharya; Richard D James
Journal:  Science       Date:  2005-01-07       Impact factor: 47.728

Review 6.  An introduction to cell motility for the physical scientist.

Authors:  Daniel A Fletcher; Julie A Theriot
Journal:  Phys Biol       Date:  2004-06       Impact factor: 2.583

7.  Shaping of elastic sheets by prescription of non-Euclidean metrics.

Authors:  Yael Klein; Efi Efrati; Eran Sharon
Journal:  Science       Date:  2007-02-23       Impact factor: 47.728

Review 8.  Macroevolution of complex cytoskeletal systems in euglenids.

Authors:  Brian S Leander; Heather J Esson; Susana A Breglia
Journal:  Bioessays       Date:  2007-10       Impact factor: 4.345

9.  Dancing volvox: hydrodynamic bound states of swimming algae.

Authors:  Knut Drescher; Kyriacos C Leptos; Idan Tuval; Takuji Ishikawa; Timothy J Pedley; Raymond E Goldstein
Journal:  Phys Rev Lett       Date:  2009-04-20       Impact factor: 9.161

10.  Cascades of convergent evolution: the corresponding evolutionary histories of euglenozoans and dinoflagellates.

Authors:  Julius Lukes; Brian S Leander; Patrick J Keeling
Journal:  Proc Natl Acad Sci U S A       Date:  2009-06-15       Impact factor: 11.205

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  12 in total

1.  Three-sphere low-Reynolds-number swimmer with a passive elastic arm.

Authors:  Alessandro Montino; Antonio DeSimone
Journal:  Eur Phys J E Soft Matter       Date:  2015-05-22       Impact factor: 1.890

Review 2.  Growth and remodelling of living tissues: perspectives, challenges and opportunities.

Authors:  Davide Ambrosi; Martine Ben Amar; Christian J Cyron; Antonio DeSimone; Alain Goriely; Jay D Humphrey; Ellen Kuhl
Journal:  J R Soc Interface       Date:  2019-08-21       Impact factor: 4.118

3.  Flagellar kinematics reveals the role of environment in shaping sperm motility.

Authors:  Jeffrey S Guasto; Jonathan B Estrada; Filippo Menolascina; Lisa J Burton; Mohak Patel; Christian Franck; A E Hosoi; Richard K Zimmer; Roman Stocker
Journal:  J R Soc Interface       Date:  2020-09-09       Impact factor: 4.118

4.  Multi-parameter actuation of a neutrally stable shell: a flexible gear-less motor.

Authors:  W Hamouche; C Maurini; S Vidoli; A Vincenti
Journal:  Proc Math Phys Eng Sci       Date:  2017-08-16       Impact factor: 2.704

5.  Euglenophycin is produced in at least six species of euglenoid algae and six of seven strains of Euglena sanguinea.

Authors:  Paul V Zimba; I-Shuo Huang; Danielle Gutierrez; Woongghi Shin; Matthew S Bennett; Richard E Triemer
Journal:  Harmful Algae       Date:  2017-02-10       Impact factor: 4.273

6.  Getting in shape and swimming: the role of cortical forces and membrane heterogeneity in eukaryotic cells.

Authors:  Hao Wu; Marco Avila Ponce de León; Hans G Othmer
Journal:  J Math Biol       Date:  2018-02-26       Impact factor: 2.259

Review 7.  A Theoretical Framework for Evolutionary Cell Biology.

Authors:  Michael Lynch; Bogi Trickovic
Journal:  J Mol Biol       Date:  2020-02-19       Impact factor: 5.469

8.  Kinematics of flagellar swimming in Euglena gracilis: Helical trajectories and flagellar shapes.

Authors:  Massimiliano Rossi; Giancarlo Cicconofri; Alfred Beran; Giovanni Noselli; Antonio DeSimone
Journal:  Proc Natl Acad Sci U S A       Date:  2017-11-27       Impact factor: 11.205

9.  EuMoBot: replicating euglenoid movement in a soft robot.

Authors:  Krishna Manaswi Digumarti; Andrew T Conn; Jonathan Rossiter
Journal:  J R Soc Interface       Date:  2018-11-21       Impact factor: 4.118

10.  Swimming Euglena respond to confinement with a behavioral change enabling effective crawling.

Authors:  Giovanni Noselli; Alfred Beran; Marino Arroyo; Antonio DeSimone
Journal:  Nat Phys       Date:  2019-02-18       Impact factor: 20.034

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