Single-Molecule Structure and Topology of Kinetoplast DNA Networks

Pinyao He; Allard J. Katan; Luca Tubiana; Cees Dekker; Davide Michieletto

doi:10.48550/arXiv.2209.01293

Single-Molecule Structure and Topology of Kinetoplast DNA Networks

Pinyao He
, Allard J. Katan
, Luca Tubiana
, Cees Dekker
, Davide Michieletto (Corresponding author)

Computational and Soft Matter Physics

Publications: Contribution to journal › Article › Peer Reviewed

Abstract

Kinetoplast DNA (kDNA) is a two-dimensional Olympic-ring-like network of mutually linked DNA minicircles found in certain parasites called trypanosomes. Understanding the self-assembly and replication of this structure are not only major open questions in biology but can also inform the design of synthetic topological materials. Here, we report the first high-resolution, single-molecule study of kDNA network topology using AFM and steered molecular dynamics simulations. We map out the DNA density within the network and the distribution of linking number and valence of the minicircles. We also characterize the DNA hubs that surround the network and show that they cause a buckling transition akin to that of a 2D elastic thermal sheet in the bulk. Intriguingly, we observe a broad distribution of density and valence of the minicircles, indicating heterogeneous network structure and individualism of different kDNA structures. Finally, we estimate the 2D Young modulus of the network to be orders of magnitude smaller than that of other 2D materials. Our findings explain outstanding questions in the field and offer single-molecule insights into the properties of a unique topological material.

Original language	English
Article number	021010
Number of pages	13
Journal	Physical Review X
Volume	13
Issue number	2
DOIs	https://doi.org/10.48550/arXiv.2209.01293 https://doi.org/10.1103/PhysRevX.13.021010
Publication status	Published - Apr 2023

Funding

This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (Grant Agreement No. 947918, TAP). D. M. also acknowledges support of the Royal Society via a University Research Fellowship. L. T. acknowledges support from MIUR, Rita Levi Montalcini Grant, 2016. C. D. acknowledges support of ERC Advanced Grant No. 883684. P. H. acknowledges Professor Yunfei Chen, Professor Zhonghua Ni, and support from the China Scholarship Council (CSC201906090029). The authors acknowledge insightful discussions with Jaco van der Torre, Alice Pyne, Elisa De Llano, and Raffaello Potestio. The authors also acknowledge the contribution of the COST Action Eutopia, CA17139.

Austrian Fields of Science 2012

103015 Condensed matter
106006 Biophysics

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https://phaidra.univie.ac.at/o:2062985Licence: CC BY 4.0

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title = "Single-Molecule Structure and Topology of Kinetoplast DNA Networks",

abstract = "Kinetoplast DNA (kDNA) is a two-dimensional Olympic-ring-like network of mutually linked DNA minicircles found in certain parasites called trypanosomes. Understanding the self-assembly and replication of this structure are not only major open questions in biology but can also inform the design of synthetic topological materials. Here, we report the first high-resolution, single-molecule study of kDNA network topology using AFM and steered molecular dynamics simulations. We map out the DNA density within the network and the distribution of linking number and valence of the minicircles. We also characterize the DNA hubs that surround the network and show that they cause a buckling transition akin to that of a 2D elastic thermal sheet in the bulk. Intriguingly, we observe a broad distribution of density and valence of the minicircles, indicating heterogeneous network structure and individualism of different kDNA structures. Finally, we estimate the 2D Young modulus of the network to be orders of magnitude smaller than that of other 2D materials. Our findings explain outstanding questions in the field and offer single-molecule insights into the properties of a unique topological material. ",

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N2 - Kinetoplast DNA (kDNA) is a two-dimensional Olympic-ring-like network of mutually linked DNA minicircles found in certain parasites called trypanosomes. Understanding the self-assembly and replication of this structure are not only major open questions in biology but can also inform the design of synthetic topological materials. Here, we report the first high-resolution, single-molecule study of kDNA network topology using AFM and steered molecular dynamics simulations. We map out the DNA density within the network and the distribution of linking number and valence of the minicircles. We also characterize the DNA hubs that surround the network and show that they cause a buckling transition akin to that of a 2D elastic thermal sheet in the bulk. Intriguingly, we observe a broad distribution of density and valence of the minicircles, indicating heterogeneous network structure and individualism of different kDNA structures. Finally, we estimate the 2D Young modulus of the network to be orders of magnitude smaller than that of other 2D materials. Our findings explain outstanding questions in the field and offer single-molecule insights into the properties of a unique topological material.

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Single-Molecule Structure and Topology of Kinetoplast DNA Networks

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Funding

Austrian Fields of Science 2012

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