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Title: Inchworm movement of two rings switching onto a thread by biased Brownian diffusion represent a three-body problem

Abstract

The coordinated motion of many individual components underpins the operation of all machines. However, despite generations of experience in engineering, understanding the motion of three or more coupled components remains a challenge, known since the time of Newton as the “three-body problem.” Here, we describe, quantify, and simulate a molecular three-body problem of threading two molecular rings onto a linear molecular thread. Specifically, we use voltage-triggered reduction of a tetrazine-based thread to capture two cyanostar macrocycles and form a [3]pseudorotaxane product. As a consequence of the noncovalent coupling between the cyanostar rings, we find the threading occurs by an unexpected and rare inchworm-like motion where one ring follows the other. The mechanism was derived from controls, analysis of cyclic voltammetry (CV) traces, and Brownian dynamics simulations. CVs from two noncovalently interacting rings match that of two covalently linked rings designed to thread via the inchworm pathway, and they deviate considerably from the CV of a macrocycle designed to thread via a stepwise pathway. Time-dependent electrochemistry provides estimates of rate constants for threading. Experimentally derived parameters (energy wells, barriers, diffusion coefficients) helped determine likely pathways of motion with rate-kinetics and Brownian dynamics simulations. Simulations verified intercomponent coupling could be separated intomore » ring–thread interactions for kinetics, and ring–ring interactions for thermodynamics to reduce the three-body problem to a two-body one. Our findings provide a basis for high-throughput design of molecular machinery with multiple components undergoing coupled motion.« less

Authors:
; ; ; ; ; ORCiD logo; ; ORCiD logo
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); UT-Battelle LLC/ORNL, Oak Ridge, TN (Unted States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1458780
Alternate Identifier(s):
OSTI ID: 1565682
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 115 Journal Issue: 38; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
74 ATOMIC AND MOLECULAR PHYSICS; Science & Technology

Citation Formats

Benson, Christopher R., Maffeo, Christopher, Fatila, Elisabeth M., Liu, Yun, Sheetz, Edward G., Aksimentiev, Aleksei, Singharoy, Abhishek, and Flood, Amar H. Inchworm movement of two rings switching onto a thread by biased Brownian diffusion represent a three-body problem. United States: N. p., 2018. Web. doi:10.1073/pnas.1719539115.
Benson, Christopher R., Maffeo, Christopher, Fatila, Elisabeth M., Liu, Yun, Sheetz, Edward G., Aksimentiev, Aleksei, Singharoy, Abhishek, & Flood, Amar H. Inchworm movement of two rings switching onto a thread by biased Brownian diffusion represent a three-body problem. United States. doi:10.1073/pnas.1719539115.
Benson, Christopher R., Maffeo, Christopher, Fatila, Elisabeth M., Liu, Yun, Sheetz, Edward G., Aksimentiev, Aleksei, Singharoy, Abhishek, and Flood, Amar H. Mon . "Inchworm movement of two rings switching onto a thread by biased Brownian diffusion represent a three-body problem". United States. doi:10.1073/pnas.1719539115.
@article{osti_1458780,
title = {Inchworm movement of two rings switching onto a thread by biased Brownian diffusion represent a three-body problem},
author = {Benson, Christopher R. and Maffeo, Christopher and Fatila, Elisabeth M. and Liu, Yun and Sheetz, Edward G. and Aksimentiev, Aleksei and Singharoy, Abhishek and Flood, Amar H.},
abstractNote = {The coordinated motion of many individual components underpins the operation of all machines. However, despite generations of experience in engineering, understanding the motion of three or more coupled components remains a challenge, known since the time of Newton as the “three-body problem.” Here, we describe, quantify, and simulate a molecular three-body problem of threading two molecular rings onto a linear molecular thread. Specifically, we use voltage-triggered reduction of a tetrazine-based thread to capture two cyanostar macrocycles and form a [3]pseudorotaxane product. As a consequence of the noncovalent coupling between the cyanostar rings, we find the threading occurs by an unexpected and rare inchworm-like motion where one ring follows the other. The mechanism was derived from controls, analysis of cyclic voltammetry (CV) traces, and Brownian dynamics simulations. CVs from two noncovalently interacting rings match that of two covalently linked rings designed to thread via the inchworm pathway, and they deviate considerably from the CV of a macrocycle designed to thread via a stepwise pathway. Time-dependent electrochemistry provides estimates of rate constants for threading. Experimentally derived parameters (energy wells, barriers, diffusion coefficients) helped determine likely pathways of motion with rate-kinetics and Brownian dynamics simulations. Simulations verified intercomponent coupling could be separated into ring–thread interactions for kinetics, and ring–ring interactions for thermodynamics to reduce the three-body problem to a two-body one. Our findings provide a basis for high-throughput design of molecular machinery with multiple components undergoing coupled motion.},
doi = {10.1073/pnas.1719539115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 38,
volume = 115,
place = {United States},
year = {2018},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1073/pnas.1719539115

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