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A nanoscale reciprocating rotary mechanism with coordinated mobility control

Biological molecular motors transform chemical energy into mechanical work by coupling cyclic catalytic reactions to large-scale structural transitions. Mechanical deformation can be surprisingly efficient in realizing such coupling, as demonstrated by the F(1)F(O) ATP synthase. Here, we describe a...

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Autores principales: Bertosin, Eva, Maffeo, Christopher M., Drexler, Thomas, Honemann, Maximilian N., Aksimentiev, Aleksei, Dietz, Hendrik
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8654862/
https://www.ncbi.nlm.nih.gov/pubmed/34880226
http://dx.doi.org/10.1038/s41467-021-27230-7
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author Bertosin, Eva
Maffeo, Christopher M.
Drexler, Thomas
Honemann, Maximilian N.
Aksimentiev, Aleksei
Dietz, Hendrik
author_facet Bertosin, Eva
Maffeo, Christopher M.
Drexler, Thomas
Honemann, Maximilian N.
Aksimentiev, Aleksei
Dietz, Hendrik
author_sort Bertosin, Eva
collection PubMed
description Biological molecular motors transform chemical energy into mechanical work by coupling cyclic catalytic reactions to large-scale structural transitions. Mechanical deformation can be surprisingly efficient in realizing such coupling, as demonstrated by the F(1)F(O) ATP synthase. Here, we describe a synthetic molecular mechanism that transforms a rotary motion of an asymmetric camshaft into reciprocating large-scale transitions in a surrounding stator orchestrated by mechanical deformation. We design the mechanism using DNA origami, characterize its structure via cryo-electron microscopy, and examine its dynamic behavior using single-particle fluorescence microscopy and molecular dynamics simulations. While the camshaft can rotate inside the stator by diffusion, the stator’s mechanics makes the camshaft pause at preferred orientations. By changing the stator’s mechanical stiffness, we accelerate or suppress the Brownian rotation, demonstrating an allosteric coupling between the camshaft and the stator. Our mechanism provides a framework for manufacturing artificial nanomachines that function because of coordinated movements of their components.
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spelling pubmed-86548622021-12-27 A nanoscale reciprocating rotary mechanism with coordinated mobility control Bertosin, Eva Maffeo, Christopher M. Drexler, Thomas Honemann, Maximilian N. Aksimentiev, Aleksei Dietz, Hendrik Nat Commun Article Biological molecular motors transform chemical energy into mechanical work by coupling cyclic catalytic reactions to large-scale structural transitions. Mechanical deformation can be surprisingly efficient in realizing such coupling, as demonstrated by the F(1)F(O) ATP synthase. Here, we describe a synthetic molecular mechanism that transforms a rotary motion of an asymmetric camshaft into reciprocating large-scale transitions in a surrounding stator orchestrated by mechanical deformation. We design the mechanism using DNA origami, characterize its structure via cryo-electron microscopy, and examine its dynamic behavior using single-particle fluorescence microscopy and molecular dynamics simulations. While the camshaft can rotate inside the stator by diffusion, the stator’s mechanics makes the camshaft pause at preferred orientations. By changing the stator’s mechanical stiffness, we accelerate or suppress the Brownian rotation, demonstrating an allosteric coupling between the camshaft and the stator. Our mechanism provides a framework for manufacturing artificial nanomachines that function because of coordinated movements of their components. Nature Publishing Group UK 2021-12-08 /pmc/articles/PMC8654862/ /pubmed/34880226 http://dx.doi.org/10.1038/s41467-021-27230-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Bertosin, Eva
Maffeo, Christopher M.
Drexler, Thomas
Honemann, Maximilian N.
Aksimentiev, Aleksei
Dietz, Hendrik
A nanoscale reciprocating rotary mechanism with coordinated mobility control
title A nanoscale reciprocating rotary mechanism with coordinated mobility control
title_full A nanoscale reciprocating rotary mechanism with coordinated mobility control
title_fullStr A nanoscale reciprocating rotary mechanism with coordinated mobility control
title_full_unstemmed A nanoscale reciprocating rotary mechanism with coordinated mobility control
title_short A nanoscale reciprocating rotary mechanism with coordinated mobility control
title_sort nanoscale reciprocating rotary mechanism with coordinated mobility control
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8654862/
https://www.ncbi.nlm.nih.gov/pubmed/34880226
http://dx.doi.org/10.1038/s41467-021-27230-7
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