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Confinement anisotropy drives polar organization of two DNA molecules interacting in a nanoscale cavity

There is growing appreciation for the role phase transition based phenomena play in biological systems. In particular, self-avoiding polymer chains are predicted to undergo a unique confinement dependent demixing transition as the anisotropy of the confined space is increased. This phenomenon may be...

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Autores principales: Liu, Zezhou, Capaldi, Xavier, Zeng, Lili, Zhang, Yuning, Reyes-Lamothe, Rodrigo, Reisner, Walter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9334635/
https://www.ncbi.nlm.nih.gov/pubmed/35902565
http://dx.doi.org/10.1038/s41467-022-31398-x
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author Liu, Zezhou
Capaldi, Xavier
Zeng, Lili
Zhang, Yuning
Reyes-Lamothe, Rodrigo
Reisner, Walter
author_facet Liu, Zezhou
Capaldi, Xavier
Zeng, Lili
Zhang, Yuning
Reyes-Lamothe, Rodrigo
Reisner, Walter
author_sort Liu, Zezhou
collection PubMed
description There is growing appreciation for the role phase transition based phenomena play in biological systems. In particular, self-avoiding polymer chains are predicted to undergo a unique confinement dependent demixing transition as the anisotropy of the confined space is increased. This phenomenon may be relevant for understanding how interactions between multiple dsDNA molecules can induce self-organized structure in prokaryotes. While recent in vivo experiments and Monte Carlo simulations have delivered essential insights into this phenomenon and its relation to bacteria, there are fundamental questions remaining concerning how segregated polymer states arise, the role of confinement anisotropy and the nature of the dynamics in the segregated states. To address these questions, we introduce an artificial nanofluidic model to quantify the interactions of multiple dsDNA molecules in cavities with controlled anisotropy. We find that two dsDNA molecules of equal size confined in an elliptical cavity will spontaneously demix and orient along the cavity poles as cavity eccentricity is increased; the two chains will then swap pole positions with a frequency that decreases with increasing cavity eccentricity. In addition, we explore a system consisting of a large dsDNA molecule and a plasmid molecule. We find that the plasmid is excluded from the larger molecule and will exhibit a preference for the ellipse poles, giving rise to a non-uniform spatial distribution in the cavity that may help explain the non-uniform plasmid distribution observed during in vivo imaging of high-copy number plasmids in bacteria.
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spelling pubmed-93346352022-07-30 Confinement anisotropy drives polar organization of two DNA molecules interacting in a nanoscale cavity Liu, Zezhou Capaldi, Xavier Zeng, Lili Zhang, Yuning Reyes-Lamothe, Rodrigo Reisner, Walter Nat Commun Article There is growing appreciation for the role phase transition based phenomena play in biological systems. In particular, self-avoiding polymer chains are predicted to undergo a unique confinement dependent demixing transition as the anisotropy of the confined space is increased. This phenomenon may be relevant for understanding how interactions between multiple dsDNA molecules can induce self-organized structure in prokaryotes. While recent in vivo experiments and Monte Carlo simulations have delivered essential insights into this phenomenon and its relation to bacteria, there are fundamental questions remaining concerning how segregated polymer states arise, the role of confinement anisotropy and the nature of the dynamics in the segregated states. To address these questions, we introduce an artificial nanofluidic model to quantify the interactions of multiple dsDNA molecules in cavities with controlled anisotropy. We find that two dsDNA molecules of equal size confined in an elliptical cavity will spontaneously demix and orient along the cavity poles as cavity eccentricity is increased; the two chains will then swap pole positions with a frequency that decreases with increasing cavity eccentricity. In addition, we explore a system consisting of a large dsDNA molecule and a plasmid molecule. We find that the plasmid is excluded from the larger molecule and will exhibit a preference for the ellipse poles, giving rise to a non-uniform spatial distribution in the cavity that may help explain the non-uniform plasmid distribution observed during in vivo imaging of high-copy number plasmids in bacteria. Nature Publishing Group UK 2022-07-28 /pmc/articles/PMC9334635/ /pubmed/35902565 http://dx.doi.org/10.1038/s41467-022-31398-x Text en © The Author(s) 2022 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
Liu, Zezhou
Capaldi, Xavier
Zeng, Lili
Zhang, Yuning
Reyes-Lamothe, Rodrigo
Reisner, Walter
Confinement anisotropy drives polar organization of two DNA molecules interacting in a nanoscale cavity
title Confinement anisotropy drives polar organization of two DNA molecules interacting in a nanoscale cavity
title_full Confinement anisotropy drives polar organization of two DNA molecules interacting in a nanoscale cavity
title_fullStr Confinement anisotropy drives polar organization of two DNA molecules interacting in a nanoscale cavity
title_full_unstemmed Confinement anisotropy drives polar organization of two DNA molecules interacting in a nanoscale cavity
title_short Confinement anisotropy drives polar organization of two DNA molecules interacting in a nanoscale cavity
title_sort confinement anisotropy drives polar organization of two dna molecules interacting in a nanoscale cavity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9334635/
https://www.ncbi.nlm.nih.gov/pubmed/35902565
http://dx.doi.org/10.1038/s41467-022-31398-x
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