Nonequilibrium sensing and its analogy to kinetic proofreading

For a paradigmatic model of chemotaxis, we analyze the effect of how a nonzero affinity driving receptors out of equilibrium affects sensitivity. This affinity arises whenever changes in receptor activity involve adenosine triphosphate hydrolysis. The sensitivity integrated over a ligand concentration range is shown to be enhanced by the affinity, providing a measure of how much energy consumption improves sensing. With this integrated sensitivity we can establish an intriguing analogy between sensing with nonequilibrium receptors and kinetic proofreading: the increase in integrated sensitivity is equivalent to the decrease of the error in kinetic proofreading. The influence of the occupancy of the receptor on the phosphorylation and dephosphorylation reaction rates is shown to be crucial for the relation between integrated sensitivity and affinity. This influence can even lead to a regime where a nonzero affinity decreases the integrated sensitivity, which corresponds to anti-proofreading.

[1]  Monica L. Skoge,et al.  Chemical sensing by nonequilibrium cooperative receptors. , 2013, Physical review letters.

[2]  David J Schwab,et al.  Energetic costs of cellular computation , 2012, Proceedings of the National Academy of Sciences.

[3]  Yuhai Tu,et al.  The nonequilibrium mechanism for ultrasensitivity in a biological switch: Sensing by Maxwell's demons , 2008, Proceedings of the National Academy of Sciences.

[4]  Pieter Rein ten Wolde,et al.  Energy dissipation and noise correlations in biochemical sensing. , 2014, Physical review letters.

[5]  H. Berg,et al.  Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking , 1972, Nature.

[6]  Stanislas Leibler,et al.  Speed, dissipation, and error in kinetic proofreading , 2012, Proceedings of the National Academy of Sciences.

[7]  C. MacPhee,et al.  Modelling amyloid fibril formation kinetics: mechanisms of nucleation and growth , 2013, Journal of physics. Condensed matter : an Institute of Physics journal.

[8]  H. Qian Cooperativity and specificity in enzyme kinetics: a single-molecule time-based perspective. , 2008, Biophysical journal.

[9]  Sarah Marzen,et al.  Statistical mechanics of Monod-Wyman-Changeux (MWC) models. , 2013, Journal of molecular biology.

[10]  Massimiliano Esposito,et al.  Erratum: Stochastic thermodynamics under coarse graining [Phys. Rev. E 85, 041125 (2012)] , 2012 .

[11]  J. Hopfield Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. C. Barato,et al.  Information-theoretic vs. thermodynamic entropy production in autonomous sensory networks , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[13]  J. Ninio Kinetic amplification of enzyme discrimination. , 1975, Biochimie.

[14]  J. Changeux,et al.  ON THE NATURE OF ALLOSTERIC TRANSITIONS: A PLAUSIBLE MODEL. , 1965, Journal of molecular biology.

[15]  C Blomberg,et al.  Thermodynamic constraints on kinetic proofreading in biosynthetic pathways. , 1980, Biophysical journal.

[16]  J. Schnakenberg Network theory of microscopic and macroscopic behavior of master equation systems , 1976 .

[17]  Yuhai Tu,et al.  The energy-speed-accuracy tradeoff in sensory adaptation , 2012, Nature Physics.

[18]  P. R. ten Wolde,et al.  Optimal resource allocation in cellular sensing systems , 2014, Proceedings of the National Academy of Sciences.

[19]  P. Gräber,et al.  Free Energy Transduction and Biochemical Cycle Kinetics. , 1990 .

[20]  Kinetic versus energetic discrimination in biological copying. , 2012, Physical review letters.

[21]  Hong Qian,et al.  Nonequilibrium thermodynamics and nonlinear kinetics in a cellular signaling switch. , 2005, Physical review letters.

[22]  Andre C. Barato,et al.  Efficiency of cellular information processing , 2014, 1405.7241.

[23]  U. Seifert Stochastic thermodynamics, fluctuation theorems and molecular machines , 2012, Reports on progress in physics. Physical Society.

[24]  M. Esposito Stochastic thermodynamics under coarse graining. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[25]  Howard C. Berg,et al.  E. coli in Motion , 2003 .

[26]  Jordan M. Horowitz,et al.  Thermodynamic Costs of Information Processing in Sensory Adaptation , 2014, PLoS Comput. Biol..

[27]  H. Qian Cyclic conformational modification of an enzyme: serial engagement, energy relay, hysteretic enzyme, and Fischer's hypothesis. , 2010, The journal of physical chemistry. B.

[28]  Marco Del Giudice,et al.  Thermodynamic limits to information harvesting by sensory systems , 2014, 1408.5128.

[29]  Charles H. Bennett,et al.  Dissipation-error tradeoff in proofreading. , 1979, Bio Systems.

[30]  Robert G. Endres,et al.  Predicting Chemical Environments of Bacteria from Receptor Signaling , 2014, PLoS Comput. Biol..

[31]  Yuhai Tu,et al.  Modeling the chemotactic response of Escherichia coli to time-varying stimuli , 2008, Proceedings of the National Academy of Sciences.

[32]  T. L. Hill,et al.  Free Energy Transduction and Biochemical Cycle Kinetics , 1988, Springer New York.

[33]  Yuhai Tu,et al.  Effects of adaptation in maintaining high sensitivity over a wide range of backgrounds for Escherichia coli chemotaxis. , 2007, Biophysical journal.

[34]  Giovanna De Palo,et al.  Unraveling Adaptation in Eukaryotic Pathways: Lessons from Protocells , 2013, PLoS Comput. Biol..

[35]  Stanislas Leibler,et al.  Discriminatory proofreading regimes in non-equilibrium systems , 2013, 1312.2286.

[36]  Hong Qian,et al.  Phosphorylation energy hypothesis: open chemical systems and their biological functions. , 2007, Annual review of physical chemistry.

[37]  Y. Tu Quantitative modeling of bacterial chemotaxis: signal amplification and accurate adaptation. , 2013, Annual review of biophysics.

[38]  Thierry Mora,et al.  Thermodynamics of statistical inference by cells. , 2014, Physical review letters.

[39]  Hong Qian,et al.  Reducing intrinsic biochemical noise in cells and its thermodynamic limit. , 2006, Journal of molecular biology.