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Motor-driven advection competes with crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites

The cytoskeleton–a composite network of biopolymers, molecular motors, and associated binding proteins–is a paradigmatic example of active matter. Particle transport through the cytoskeleton can range from anomalous and heterogeneous subdiffusion to superdiffusion and advection. Yet, recapitulating...

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Autores principales: Sheung, Janet Y., Garamella, Jonathan, Kahl, Stella K., Lee, Brian Y., McGorty, Ryan J., Robertson-Anderson, Rae M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10403238/
https://www.ncbi.nlm.nih.gov/pubmed/37547053
http://dx.doi.org/10.3389/fphy.2022.1055441
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author Sheung, Janet Y.
Garamella, Jonathan
Kahl, Stella K.
Lee, Brian Y.
McGorty, Ryan J.
Robertson-Anderson, Rae M.
author_facet Sheung, Janet Y.
Garamella, Jonathan
Kahl, Stella K.
Lee, Brian Y.
McGorty, Ryan J.
Robertson-Anderson, Rae M.
author_sort Sheung, Janet Y.
collection PubMed
description The cytoskeleton–a composite network of biopolymers, molecular motors, and associated binding proteins–is a paradigmatic example of active matter. Particle transport through the cytoskeleton can range from anomalous and heterogeneous subdiffusion to superdiffusion and advection. Yet, recapitulating and understanding these properties–ubiquitous to the cytoskeleton and other out-of-equilibrium soft matter systems–remains challenging. Here, we combine light sheet microscopy with differential dynamic microscopy and single-particle tracking to elucidate anomalous and advective transport in actomyosin-microtubule composites. We show that particles exhibit multi-mode transport that transitions from pronounced subdiffusion to superdiffusion at tunable crossover timescales. Surprisingly, while higher actomyosin content increases the range of timescales over which transport is superdiffusive, it also markedly increases the degree of subdiffusion at short timescales and generally slows transport. Corresponding displacement distributions display unique combinations of non-Gaussianity, asymmetry, and non-zero modes, indicative of directed advection coupled with caged diffusion and hopping. At larger spatiotemporal scales, particles in active composites exhibit superdiffusive dynamics with scaling exponents that are robust to changing actomyosin fractions, in contrast to normal, yet faster, diffusion in networks without actomyosin. Our specific results shed important new light on the interplay between non-equilibrium processes, crowding and heterogeneity in active cytoskeletal systems. More generally, our approach is broadly applicable to active matter systems to elucidate transport and dynamics across scales.
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spelling pubmed-104032382023-08-04 Motor-driven advection competes with crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites Sheung, Janet Y. Garamella, Jonathan Kahl, Stella K. Lee, Brian Y. McGorty, Ryan J. Robertson-Anderson, Rae M. Front Phys Article The cytoskeleton–a composite network of biopolymers, molecular motors, and associated binding proteins–is a paradigmatic example of active matter. Particle transport through the cytoskeleton can range from anomalous and heterogeneous subdiffusion to superdiffusion and advection. Yet, recapitulating and understanding these properties–ubiquitous to the cytoskeleton and other out-of-equilibrium soft matter systems–remains challenging. Here, we combine light sheet microscopy with differential dynamic microscopy and single-particle tracking to elucidate anomalous and advective transport in actomyosin-microtubule composites. We show that particles exhibit multi-mode transport that transitions from pronounced subdiffusion to superdiffusion at tunable crossover timescales. Surprisingly, while higher actomyosin content increases the range of timescales over which transport is superdiffusive, it also markedly increases the degree of subdiffusion at short timescales and generally slows transport. Corresponding displacement distributions display unique combinations of non-Gaussianity, asymmetry, and non-zero modes, indicative of directed advection coupled with caged diffusion and hopping. At larger spatiotemporal scales, particles in active composites exhibit superdiffusive dynamics with scaling exponents that are robust to changing actomyosin fractions, in contrast to normal, yet faster, diffusion in networks without actomyosin. Our specific results shed important new light on the interplay between non-equilibrium processes, crowding and heterogeneity in active cytoskeletal systems. More generally, our approach is broadly applicable to active matter systems to elucidate transport and dynamics across scales. 2022 2022-11-18 /pmc/articles/PMC10403238/ /pubmed/37547053 http://dx.doi.org/10.3389/fphy.2022.1055441 Text en https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) (https://creativecommons.org/licenses/by/4.0/) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Article
Sheung, Janet Y.
Garamella, Jonathan
Kahl, Stella K.
Lee, Brian Y.
McGorty, Ryan J.
Robertson-Anderson, Rae M.
Motor-driven advection competes with crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites
title Motor-driven advection competes with crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites
title_full Motor-driven advection competes with crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites
title_fullStr Motor-driven advection competes with crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites
title_full_unstemmed Motor-driven advection competes with crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites
title_short Motor-driven advection competes with crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites
title_sort motor-driven advection competes with crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10403238/
https://www.ncbi.nlm.nih.gov/pubmed/37547053
http://dx.doi.org/10.3389/fphy.2022.1055441
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