Literature DB >> 24411242

Evidence for two extremes of ciliary motor response in a single swimming microorganism.

Ilyong Jung1, Thomas R Powers2, James M Valles3.   

Abstract

Because arrays of motile cilia drive fluids for a range of processes, the versatile mechano-chemical mechanism coordinating them has been under scrutiny. The protist Paramecium presents opportunities to compare how groups of cilia perform two distinct functions, swimming propulsion and nutrient uptake. We present how the body cilia responsible for propulsion and the oral-groove cilia responsible for nutrient uptake respond to changes in their mechanical environment accomplished by varying the fluid viscosity over a factor of 7. Analysis with a phenomenological model of trajectories of swimmers made neutrally buoyant with magnetic forces combined with high-speed imaging of ciliary beating reveal that the body cilia exert a nearly constant propulsive force primarily by reducing their beat frequency as viscosity increases. By contrast, the oral-groove cilia beat at a nearly constant frequency. The existence of two extremes of motor response in a unicellular organism prompts unique investigations of factors controlling ciliary beating.
Copyright © 2014 Biophysical Society. Published by Elsevier Inc. All rights reserved.

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Year:  2014        PMID: 24411242      PMCID: PMC3907369          DOI: 10.1016/j.bpj.2013.11.3703

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  32 in total

1.  Kinematics of helical motion of microorganisms capable of motion with four degrees of freedom.

Authors:  H C Crenshaw
Journal:  Biophys J       Date:  1989-11       Impact factor: 4.033

2.  An axonemal dynein particularly important for flagellar movement at high viscosity. Implications from a new Chlamydomonas mutant deficient in the dynein heavy chain gene DHC9.

Authors:  Toshiki Yagi; Itsushi Minoura; Akiko Fujiwara; Ryo Saito; Takuo Yasunaga; Masafumi Hirono; Ritsu Kamiya
Journal:  J Biol Chem       Date:  2005-10-18       Impact factor: 5.157

3.  An integrative computational model of multiciliary beating.

Authors:  Xingzhou Yang; Robert H Dillon; Lisa J Fauci
Journal:  Bull Math Biol       Date:  2008-01-31       Impact factor: 1.758

4.  Theory of swimming filaments in viscoelastic media.

Authors:  Henry C Fu; Thomas R Powers; Charles W Wolgemuth
Journal:  Phys Rev Lett       Date:  2007-12-19       Impact factor: 9.161

5.  Autoregulation of beat frequency in respiratory ciliated cells. Demonstration by viscous loading.

Authors:  N T Johnson; M Villalón; F H Royce; R Hard; P Verdugo
Journal:  Am Rev Respir Dis       Date:  1991-11

6.  Outer dynein arm light chain 1 is essential for controlling the ciliary response to cyclic AMP in Paramecium tetraurelia.

Authors:  Osamu Kutomi; Manabu Hori; Masaki Ishida; Takashi Tominaga; Hiroyuki Kamachi; France Koll; Jean Cohen; Norico Yamada; Munenori Noguchi
Journal:  Eukaryot Cell       Date:  2012-03-16

7.  Swimming Paramecium in magnetically simulated enhanced, reduced, and inverted gravity environments.

Authors:  Karine Guevorkian; James M Valles
Journal:  Proc Natl Acad Sci U S A       Date:  2006-08-17       Impact factor: 11.205

8.  Low flagellar motor torque and high swimming efficiency of Caulobacter crescentus swarmer cells.

Authors:  Guanglai Li; Jay X Tang
Journal:  Biophys J       Date:  2006-07-14       Impact factor: 4.033

9.  An outer arm Dynein conformational switch is required for metachronal synchrony of motile cilia in planaria.

Authors:  Panteleimon Rompolas; Ramila S Patel-King; Stephen M King
Journal:  Mol Biol Cell       Date:  2010-09-15       Impact factor: 4.138

10.  The effect of viscous loading on brain ependymal cilia.

Authors:  Christopher Liam O'Callaghan; Kulvinder Sikand; Andrew Rutman; Robert Anthony Hirst
Journal:  Neurosci Lett       Date:  2008-05-02       Impact factor: 3.046

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  9 in total

1.  Use of a novel cell adhesion method and digital measurement to show stimulus-dependent variation in somatic and oral ciliary beat frequency in Paramecium.

Authors:  Wade E Bell; Richard Hallworth; Todd A Wyatt; Joseph H Sisson
Journal:  J Eukaryot Microbiol       Date:  2014-08-21       Impact factor: 3.346

2.  Walking is like slithering: A unifying, data-driven view of locomotion.

Authors:  Dan Zhao; Brian Bittner; Glenna Clifton; Nick Gravish; Shai Revzen
Journal:  Proc Natl Acad Sci U S A       Date:  2022-09-06       Impact factor: 12.779

Review 3.  Integrative Neuroscience of Paramecium, a "Swimming Neuron".

Authors:  Romain Brette
Journal:  eNeuro       Date:  2021-06-07

4.  DisAp-dependent striated fiber elongation is required to organize ciliary arrays.

Authors:  Domenico F Galati; Stephanie Bonney; Zev Kronenberg; Christina Clarissa; Mark Yandell; Nels C Elde; Maria Jerka-Dziadosz; Thomas H Giddings; Joseph Frankel; Chad G Pearson
Journal:  J Cell Biol       Date:  2014-12-22       Impact factor: 10.539

5.  Mobile Diagnostics Based on Motion? A Close Look at Motility Patterns in the Schistosome Life Cycle.

Authors:  Ewert Linder; Sami Varjo; Cecilia Thors
Journal:  Diagnostics (Basel)       Date:  2016-06-17

6.  Swimming eukaryotic microorganisms exhibit a universal speed distribution.

Authors:  Maciej Lisicki; Marcos F Velho Rodrigues; Raymond E Goldstein; Eric Lauga
Journal:  Elife       Date:  2019-07-16       Impact factor: 8.140

Review 7.  Polarity in Ciliate Models: From Cilia to Cell Architecture.

Authors:  Helena Soares; Bruno Carmona; Sofia Nolasco; Luís Viseu Melo
Journal:  Front Cell Dev Biol       Date:  2019-10-18

8.  Three-dimensional tracking of the ciliate Tetrahymena reveals the mechanism of ciliary stroke-driven helical swimming.

Authors:  Akisato Marumo; Masahiko Yamagishi; Junichiro Yajima
Journal:  Commun Biol       Date:  2021-10-21

9.  Somersault of Paramecium in extremely confined environments.

Authors:  Saikat Jana; Aja Eddins; Corrie Spoon; Sunghwan Jung
Journal:  Sci Rep       Date:  2015-08-19       Impact factor: 4.379

  9 in total

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