Morphological transitions of elastic filaments in shear flow
The morphological dynamics, instabilities, and transitions of elastic filaments in viscous flows underlie a wealth of biophysical processes from flagellar propulsion to intracellular streaming and are also key to deciphering the rheological behavior of many complex fluids and soft materials. Here, w...
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Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 115; no. 38; pp. 9438 - 9443 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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United States
National Academy of Sciences
18.09.2018
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Abstract | The morphological dynamics, instabilities, and transitions of elastic filaments in viscous flows underlie a wealth of biophysical processes from flagellar propulsion to intracellular streaming and are also key to deciphering the rheological behavior of many complex fluids and soft materials. Here, we combine experiments and computational modeling to elucidate the dynamical regimes and morphological transitions of elastic Brownian filaments in a simple shear flow. Actin filaments are used as an experimental model system and their conformations are investigated through fluorescence microscopy in microfluidic channels. Simulations matching the experimental conditions are also performed using inextensible Euler–Bernoulli beam theory and nonlocal slender-body hydrodynamics in the presence of thermal fluctuations and agree quantitatively with observations. We demonstrate that filament dynamics in this system are primarily governed by a dimensionless elasto-viscous number comparing viscous drag forces to elastic bending forces, with thermal fluctuations playing only a secondary role. While short and rigid filaments perform quasi-periodic tumbling motions, a buckling instability arises above a critical flow strength. A second transition to strongly deformed shapes occurs at a yet larger value of the elasto-viscous number and is characterized by the appearance of localized high-curvature bends that propagate along the filaments in apparent “snaking” motions. A theoretical model for the as yet unexplored onset of snaking accurately predicts the transition and explains the observed dynamics. We present a complete characterization of filament morphologies and transitions as a function of elasto-viscous number and scaled persistence length and demonstrate excellent agreement between theory, experiments, and simulations. |
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AbstractList | The morphological dynamics, instabilities and transitions of elastic filaments in viscous flows underlie a wealth of biophysical processes from flagellar propulsion to intracellular streaming, and are also key to deciphering the rheological behavior of many complex fluids and soft materials. Here, we combine experiments and computational modeling to elucidate the dynamical regimes and morphological transitions of elastic Brownian filaments in a simple shear flow. Actin filaments are employed as an experimental model system and their conformations are investigated through fluorescence microscopy in microfluidic channels. Simulations matching the experimental conditions are also performed using inextensible Euler-Bernoulli beam theory and non-local slender-body hydrodynamics in the presence of thermal fluctuations, and agree quantitatively with observations. We demonstrate that filament dynamics in this system is primarily governed by a dimensionless elasto-viscous number comparing viscous drag forces to elastic bending forces, with thermal fluctuations only playing a secondary role. While short and rigid filaments perform quasi-periodic tumbling motions, a buckling instability arises above a critical flow strength. A second transition to strongly-deformed shapes occurs at a yet larger value of the elasto-viscous number and is characterized by the appearance of localized high-curvature bends that propagate along the filaments in apparent "snaking" motions. A theoretical model for the so far unexplored onset of snaking accurately predicts the transition and explains the observed dynamics. We present a complete characterization of filament morphologies and transitions as a function of elasto-viscous number and scaled persistence length and demonstrate excellent agreement between theory, experiments and simulations. The morphological dynamics, instabilities, and transitions of elastic filaments in viscous flows underlie a wealth of biophysical processes from flagellar propulsion to intracellular streaming and are also key to deciphering the rheological behavior of many complex fluids and soft materials. Here, we combine experiments and computational modeling to elucidate the dynamical regimes and morphological transitions of elastic Brownian filaments in a simple shear flow. Actin filaments are used as an experimental model system and their conformations are investigated through fluorescence microscopy in microfluidic channels. Simulations matching the experimental conditions are also performed using inextensible Euler-Bernoulli beam theory and nonlocal slender-body hydrodynamics in the presence of thermal fluctuations and agree quantitatively with observations. We demonstrate that filament dynamics in this system are primarily governed by a dimensionless elasto-viscous number comparing viscous drag forces to elastic bending forces, with thermal fluctuations playing only a secondary role. While short and rigid filaments perform quasi-periodic tumbling motions, a buckling instability arises above a critical flow strength. A second transition to strongly deformed shapes occurs at a yet larger value of the elasto-viscous number and is characterized by the appearance of localized high-curvature bends that propagate along the filaments in apparent "snaking" motions. A theoretical model for the as yet unexplored onset of snaking accurately predicts the transition and explains the observed dynamics. We present a complete characterization of filament morphologies and transitions as a function of elasto-viscous number and scaled persistence length and demonstrate excellent agreement between theory, experiments, and simulations. The morphological dynamics, instabilities, and transitions of elastic filaments in viscous flows underlie a wealth of biophysical processes from flagellar propulsion to intracellular streaming and are also key to deciphering the rheological behavior of many complex fluids and soft materials. Here, we combine experiments and computational modeling to elucidate the dynamical regimes and morphological transitions of elastic Brownian filaments in a simple shear flow. Actin filaments are used as an experimental model system and their conformations are investigated through fluorescence microscopy in microfluidic channels. Simulations matching the experimental conditions are also performed using inextensible Euler-Bernoulli beam theory and nonlocal slender-body hydrodynamics in the presence of thermal fluctuations and agree quantitatively with observations. We demonstrate that filament dynamics in this system are primarily governed by a dimensionless elasto-viscous number comparing viscous drag forces to elastic bending forces, with thermal fluctuations playing only a secondary role. While short and rigid filaments perform quasi-periodic tumbling motions, a buckling instability arises above a critical flow strength. A second transition to strongly deformed shapes occurs at a yet larger value of the elasto-viscous number and is characterized by the appearance of localized high-curvature bends that propagate along the filaments in apparent "snaking" motions. A theoretical model for the as yet unexplored onset of snaking accurately predicts the transition and explains the observed dynamics. We present a complete characterization of filament morphologies and transitions as a function of elasto-viscous number and scaled persistence length and demonstrate excellent agreement between theory, experiments, and simulations.The morphological dynamics, instabilities, and transitions of elastic filaments in viscous flows underlie a wealth of biophysical processes from flagellar propulsion to intracellular streaming and are also key to deciphering the rheological behavior of many complex fluids and soft materials. Here, we combine experiments and computational modeling to elucidate the dynamical regimes and morphological transitions of elastic Brownian filaments in a simple shear flow. Actin filaments are used as an experimental model system and their conformations are investigated through fluorescence microscopy in microfluidic channels. Simulations matching the experimental conditions are also performed using inextensible Euler-Bernoulli beam theory and nonlocal slender-body hydrodynamics in the presence of thermal fluctuations and agree quantitatively with observations. We demonstrate that filament dynamics in this system are primarily governed by a dimensionless elasto-viscous number comparing viscous drag forces to elastic bending forces, with thermal fluctuations playing only a secondary role. While short and rigid filaments perform quasi-periodic tumbling motions, a buckling instability arises above a critical flow strength. A second transition to strongly deformed shapes occurs at a yet larger value of the elasto-viscous number and is characterized by the appearance of localized high-curvature bends that propagate along the filaments in apparent "snaking" motions. A theoretical model for the as yet unexplored onset of snaking accurately predicts the transition and explains the observed dynamics. We present a complete characterization of filament morphologies and transitions as a function of elasto-viscous number and scaled persistence length and demonstrate excellent agreement between theory, experiments, and simulations. Elastic filaments and semiflexible polymers occur ubiquitously in biophysical systems and are key components of many complex fluids, yet our understanding of their conformational dynamics under flow is incomplete. Here, we report on experimental observations of actin filaments in simple shear and characterize their various dynamical regimes from tumbling to buckling and snaking. Numerical simulations accounting for elastohydrodynamics as well as Brownian fluctuations show perfect agreement with measurements. Using a reduced-order theoretical model, we elucidate the unexplained mechanism for the transition to snaking. Our results pave the way for a better understanding of biophysical processes, as well as the rheology of sheared soft materials, and provide a theoretical framework for the exploration of the dynamics of dilute and semidilute suspensions. The morphological dynamics, instabilities, and transitions of elastic filaments in viscous flows underlie a wealth of biophysical processes from flagellar propulsion to intracellular streaming and are also key to deciphering the rheological behavior of many complex fluids and soft materials. Here, we combine experiments and computational modeling to elucidate the dynamical regimes and morphological transitions of elastic Brownian filaments in a simple shear flow. Actin filaments are used as an experimental model system and their conformations are investigated through fluorescence microscopy in microfluidic channels. Simulations matching the experimental conditions are also performed using inextensible Euler–Bernoulli beam theory and nonlocal slender-body hydrodynamics in the presence of thermal fluctuations and agree quantitatively with observations. We demonstrate that filament dynamics in this system are primarily governed by a dimensionless elasto-viscous number comparing viscous drag forces to elastic bending forces, with thermal fluctuations playing only a secondary role. While short and rigid filaments perform quasi-periodic tumbling motions, a buckling instability arises above a critical flow strength. A second transition to strongly deformed shapes occurs at a yet larger value of the elasto-viscous number and is characterized by the appearance of localized high-curvature bends that propagate along the filaments in apparent “snaking” motions. A theoretical model for the as yet unexplored onset of snaking accurately predicts the transition and explains the observed dynamics. We present a complete characterization of filament morphologies and transitions as a function of elasto-viscous number and scaled persistence length and demonstrate excellent agreement between theory, experiments, and simulations. |
Author | Lindner, Anke du Roure, Olivia Saintillan, David Chakrabarti, Brato Liu, Yanan |
Author_xml | – sequence: 1 givenname: Yanan surname: Liu fullname: Liu, Yanan organization: Physique et Mécanique des Milieux Hétérogènes (PMMH), ESPCI Paris, PSL University, CNRS, Sorbonne Université, Université Paris Diderot, 75005 Paris, France – sequence: 2 givenname: Brato surname: Chakrabarti fullname: Chakrabarti, Brato organization: Department of Mechanical and Aerospace Engineering, University of California San Diego, La Jolla, CA 92093 – sequence: 3 givenname: David surname: Saintillan fullname: Saintillan, David organization: Department of Mechanical and Aerospace Engineering, University of California San Diego, La Jolla, CA 92093 – sequence: 4 givenname: Anke surname: Lindner fullname: Lindner, Anke organization: Physique et Mécanique des Milieux Hétérogènes (PMMH), ESPCI Paris, PSL University, CNRS, Sorbonne Université, Université Paris Diderot, 75005 Paris, France – sequence: 5 givenname: Olivia surname: du Roure fullname: du Roure, Olivia organization: Physique et Mécanique des Milieux Hétérogènes (PMMH), ESPCI Paris, PSL University, CNRS, Sorbonne Université, Université Paris Diderot, 75005 Paris, France |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30181295$$D View this record in MEDLINE/PubMed https://hal.science/hal-02167915$$DView record in HAL |
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Copyright | Volumes 1–89 and 106–115, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Sep 18, 2018 Distributed under a Creative Commons Attribution 4.0 International License 2018 |
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Keywords | buckling instabilities actin filaments flexible fibers fluid structure interactions |
Language | English |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 1Y.L. and B.C. contributed equally to this work. Author contributions: Y.L., B.C., D.S., A.L., and O.d.R. designed research; Y.L., A.L., and O.d.R. performed experiments; B.C. and D.S. performed simulations; Y.L., B.C., D.S., A.L., and O.d.R. analyzed data and contributed to the theoretical model; and Y.L., B.C., D.S., A.L., and O.d.R. wrote the paper. Edited by Howard A. Stone, Princeton University, Princeton, NJ, and approved August 3, 2018 (received for review March 31, 2018) |
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Snippet | The morphological dynamics, instabilities, and transitions of elastic filaments in viscous flows underlie a wealth of biophysical processes from flagellar... Elastic filaments and semiflexible polymers occur ubiquitously in biophysical systems and are key components of many complex fluids, yet our understanding of... The morphological dynamics, instabilities and transitions of elastic filaments in viscous flows underlie a wealth of biophysical processes from flagellar... |
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SubjectTerms | Actin Actin Cytoskeleton - chemistry Actin Cytoskeleton - metabolism Algorithms Beam theory (structures) Behavior Bends Biophysical Phenomena Computational fluid dynamics Computer applications Computer Simulation Critical flow Curvature Deformation mechanisms Dimensionless numbers Drag Elastic bending Elasticity Euler-Bernoulli beams Filaments Flagella Flow stability Fluctuations Fluid Dynamics Fluid flow Fluorescence Fluorescence microscopy Hydrodynamics Mechanics Microfluidics Microscopy Microscopy, Fluorescence Models, Theoretical Molecular Conformation Morphology Motion stability Physical Sciences Physics Rheological properties Rheology Shear flow Solid mechanics Streaming Studies Thermodynamics Transitions Tumbling Viscosity Viscous drag |
Title | Morphological transitions of elastic filaments in shear flow |
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