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      Topologically protected modes in non-equilibrium stochastic systems

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      1 , 2 , a , 1 , 3
      Nature Communications
      Nature Publishing Group

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          Abstract

          Non-equilibrium driving of biophysical processes is believed to enable their robust functioning despite the presence of thermal fluctuations and other sources of disorder. Such robust functions include sensory adaptation, enhanced enzymatic specificity and maintenance of coherent oscillations. Elucidating the relation between energy consumption and organization remains an important and open question in non-equilibrium statistical mechanics. Here we report that steady states of systems with non-equilibrium fluxes can support topologically protected boundary modes that resemble similar modes in electronic and mechanical systems. Akin to their electronic and mechanical counterparts, topological-protected boundary steady states in non-equilibrium systems are robust and are largely insensitive to local perturbations. We argue that our work provides a framework for how biophysical systems can use non-equilibrium driving to achieve robust function.

          Abstract

          Energy dissipation characterizes the states far from equilibrium, whilst how it affects the local organization remains elusive. Here, Murugan et al. show that the non-equilibrium systems exhibit topologically protected boundary modes that have been known in electronic and mechanical systems.

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          Most cited references16

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          Robustness in simple biochemical networks.

          Cells use complex networks of interacting molecular components to transfer and process information. These "computational devices of living cells" are responsible for many important cellular processes, including cell-cycle regulation and signal transduction. Here we address the issue of the sensitivity of the networks to variations in their biochemical parameters. We propose a mechanism for robust adaptation in simple signal transduction networks. We show that this mechanism applies in particular to bacterial chemotaxis. This is demonstrated within a quantitative model which explains, in a unified way, many aspects of chemotaxis, including proper responses to chemical gradients. The adaptation property is a consequence of the network's connectivity and does not require the 'fine-tuning' of parameters. We argue that the key properties of biochemical networks should be robust in order to ensure their proper functioning.
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            Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity.

            J Hopfield (1974)
            The specificity with which the genetic code is read in protein synthesis, and with which other highly specific biosynthetic reactions take place, can be increased above the level available from free energy differences in intermediates or kinetic barriers by a process defined here as kinetic proofreading. A simple kinetic pathway is described which results in this proofreading when the reaction is strongly but nonspecifically driven, e.g., by phosphate hydrolysis. Protein synthesis, amino acid recognition, and DNA replication, all exhibit the features of this model. In each case, known reactions which otherwise appear to be useless or deleterious complications are seen to be essential to the proofreading function.
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              Broken detailed balance at mesoscopic scales in active biological systems

              Systems in thermodynamic equilibrium are not only characterized by time-independent macroscopic properties, but also satisfy the principle of detailed balance in the transitions between microscopic configurations. Living systems function out of equilibrium and are characterized by directed fluxes through chemical states, which violate detailed balance at the molecular scale. Here we introduce a method to probe for broken detailed balance and demonstrate how such nonequilibrium dynamics are manifest at the mesosopic scale. The periodic beating of an isolated flagellum from Chlamydomonas reinhardtii exhibits probability flux in the phase space of shapes. With a model, we show how the breaking of detailed balance can also be quantified in stationary, nonequilibrium stochastic systems in the absence of periodic motion. We further demonstrate such broken detailed balance in the nonperiodic fluctuations of primary cilia of epithelial cells. Our analysis provides a general tool to identify nonequilibrium dynamics in cells and tissues.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                10 January 2017
                2017
                : 8
                : 13881
                Affiliations
                [1 ]James Franck Institute, University of Chicago , Chicago, Illinois 60637, USA
                [2 ]Department of Physics, University of Chicago , Chicago, Illinois 60637, USA
                [3 ]Department of Chemistry, University of Chicago , Chicago, Illinois 60637, USA
                Author notes
                Article
                ncomms13881
                10.1038/ncomms13881
                5234070
                28071644
                2589425f-9ab4-4419-abe0-0988dc4f4b9a
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 07 July 2016
                : 08 November 2016
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