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      The energy-speed-accuracy tradeoff in sensory adaptation

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          Abstract

          Adaptation is the essential process by which an organism becomes better suited to its environment. The benefits of adaptation are well documented, but the cost it incurs remains poorly understood. Here, by analysing a stochastic model of a minimum feedback network underlying many sensory adaptation systems, we show that adaptive processes are necessarily dissipative, and continuous energy consumption is required to stabilize the adapted state. Our study reveals a general relation among energy dissipation rate, adaptation speed and the maximum adaptation accuracy. This energy-speed-accuracy relation is tested in the Escherichia coli chemosensory system, which exhibits near-perfect chemoreceptor adaptation. We identify key requirements for the underlying biochemical network to achieve accurate adaptation with a given energy budget. Moreover, direct measurements confirm the prediction that adaptation slows down as cells gradually de-energize in a nutrient-poor medium without compromising adaptation accuracy. Our work provides a general framework to study cost-performance tradeoffs for cellular regulatory functions and information processing.

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          Most cited references41

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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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            Defining network topologies that can achieve biochemical adaptation.

            Many signaling systems show adaptation-the ability to reset themselves after responding to a stimulus. We computationally searched all possible three-node enzyme network topologies to identify those that could perform adaptation. Only two major core topologies emerge as robust solutions: a negative feedback loop with a buffering node and an incoherent feedforward loop with a proportioner node. Minimal circuits containing these topologies are, within proper regions of parameter space, sufficient to achieve adaptation. More complex circuits that robustly perform adaptation all contain at least one of these topologies at their core. This analysis yields a design table highlighting a finite set of adaptive circuits. Despite the diversity of possible biochemical networks, it may be common to find that only a finite set of core topologies can execute a particular function. These design rules provide a framework for functionally classifying complex natural networks and a manual for engineering networks. For a video summary of this article, see the PaperFlick file with the Supplemental Data available online.
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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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                Author and article information

                Journal
                101235387
                34285
                Nat Phys
                Nature physics
                1745-2473
                29 March 2012
                25 March 2012
                1 May 2012
                01 November 2012
                : 8
                : 5
                : 422-428
                Affiliations
                [1 ]IBM T.J. Watson Research Center, P.O. Box 218, Yorktown Heights, New York 10598, USA
                [2 ]Max Planck Institute for the Physics of Complex Systems, Nothnitzer Str. 38, 01187 Dresden, Germany
                [3 ]Zentrum fur Molekulare Biologie der Universitat Heidelberg, Heidelberg, Germany
                Author notes
                [# ]Correspondence should be addressed to YT ( yuhai@ 123456us.ibm.com )
                [†]

                Present address: NCI Physical Sciences - Oncology Center, Johns Hopkins University, 3400 N Charles St., Maryland 21218, USA

                [*]

                These authors contributed equally to this work

                Article
                NIHMS359045
                10.1038/nphys2276
                3378065
                22737175
                0f4a95ac-39b2-4dd9-9dc7-dfffadcbef55

                Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

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                Physics
                sensory adaptation,adaptation speed,information processing,adaptation accuracy,energy dissipation,non-equilibrium system

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