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Title: Topology, landscapes, and biomolecular energy transport

Abstract

While ubiquitous, energy redistribution remains a poorly understood facet of the nonequilibrium thermodynamics of biomolecules. At the molecular level, finite-size effects, pronounced nonlinearities, and ballistic processes produce behavior that diverges from the macroscale. Here, we show that transient thermal transport reflects macromolecular energy landscape architecture through the topological characteristics of molecular contacts and the nonlinear processes that mediate dynamics. While the former determines transport pathways via pairwise interactions, the latter reflects frustration within the landscape for local conformational rearrangements. Unlike transport through small-molecule systems, such as alkanes, nonlinearity dominates over coherent processes at even quite short time- and length-scales. Our exhaustive all-atom simulations and novel local-in-time and space analysis, applicable to both theory and experiment, permit dissection of energy migration in biomolecules. The approach demonstrates that vibrational energy transport can probe otherwise inaccessible aspects of macromolecular dynamics and interactions that underly biological function.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]
  1. National Inst. of Standards and Technology (NIST), Gaithersburg, MD (United States); Univ. of Maryland, College Park, MD (United States)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  3. National Inst. of Standards and Technology (NIST), Gaithersburg, MD (United States)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1572330
Report Number(s):
LA-UR-19-23856
Journal ID: ISSN 2041-1723
Grant/Contract Number:  
89233218CNA000001
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Elenewski, Justin E., Velizhanin, Kirill A., and Zwolak, Michael Philip. Topology, landscapes, and biomolecular energy transport. United States: N. p., 2019. Web. doi:10.1038/s41467-019-12700-w.
Elenewski, Justin E., Velizhanin, Kirill A., & Zwolak, Michael Philip. Topology, landscapes, and biomolecular energy transport. United States. doi:10.1038/s41467-019-12700-w.
Elenewski, Justin E., Velizhanin, Kirill A., and Zwolak, Michael Philip. Fri . "Topology, landscapes, and biomolecular energy transport". United States. doi:10.1038/s41467-019-12700-w. https://www.osti.gov/servlets/purl/1572330.
@article{osti_1572330,
title = {Topology, landscapes, and biomolecular energy transport},
author = {Elenewski, Justin E. and Velizhanin, Kirill A. and Zwolak, Michael Philip},
abstractNote = {While ubiquitous, energy redistribution remains a poorly understood facet of the nonequilibrium thermodynamics of biomolecules. At the molecular level, finite-size effects, pronounced nonlinearities, and ballistic processes produce behavior that diverges from the macroscale. Here, we show that transient thermal transport reflects macromolecular energy landscape architecture through the topological characteristics of molecular contacts and the nonlinear processes that mediate dynamics. While the former determines transport pathways via pairwise interactions, the latter reflects frustration within the landscape for local conformational rearrangements. Unlike transport through small-molecule systems, such as alkanes, nonlinearity dominates over coherent processes at even quite short time- and length-scales. Our exhaustive all-atom simulations and novel local-in-time and space analysis, applicable to both theory and experiment, permit dissection of energy migration in biomolecules. The approach demonstrates that vibrational energy transport can probe otherwise inaccessible aspects of macromolecular dynamics and interactions that underly biological function.},
doi = {10.1038/s41467-019-12700-w},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {10}
}

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