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Polarizability Of The Active Site Of Cytochrome C Reduces The Activation Barrier For Electron Transfer
M. Dinpajooh, D. Martin, D. Matyushov
Published 2016 · Materials Science, Medicine
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Enzymes in biology’s energy chains operate with low energy input distributed through multiple electron transfer steps between protein active sites. The general challenge of biological design is how to lower the activation barrier without sacrificing a large negative reaction free energy. We show that this goal is achieved through a large polarizability of the active site. It is polarized by allowing a large number of excited states, which are populated quantum mechanically by electrostatic fluctuations of the protein and hydration water shells. This perspective is achieved by extensive mixed quantum mechanical/molecular dynamics simulations of the half reaction of reduction of cytochrome c. The barrier for electron transfer is consistently lowered by increasing the number of excited states included in the Hamiltonian of the active site diagonalized along the classical trajectory. We suggest that molecular polarizability, in addition to much studied electrostatics of permanent charges, is a key parameter to consider in order to understand how enzymes work.
This paper references
Interfacial Structural Transition in Hydration Shells of a Polarizable Solute.
M. Dinpajooh (2015)
The fluctuation-dissipation theorem
R. Kubo (1966)
Role of protein frame and solvent for the redox properties of azurin from Pseudomonas aeruginosa
M. Cascella (2006)
Dynamics of reactions in polar solvents. Semiclassical trajectory studies of electron-transfer and proton-transfer reactions
A. Warshel (1982)
The incorporation of quantum effects in enzyme kinetics modeling.
D. Truhlar (2002)
Protein-water electrostatics and principles of bioenergetics.
David N. LeBard (2010)
OPTICAL AND RADIATIONLESS INTRAMOLECULAR ELECTRON TRANSITIONS IN NONPOLAR FLUIDS : RELATIVE EFFECTS OF INDUCTION AND DISPERSION INTERACTIONS
D. Matyushov (1995)
Modeling the free energy surfaces of electron transfer in condensed phases
D. Matyushov (2000)
A unified model of protein dynamics
H. Frauenfelder (2009)
Computer Modeling of Chemical Reactions in Enzymes and Solutions
A. Warshel (1991)
Nonadiabatic QM/MM simulations of fast charge transfer in Escherichia coli DNA photolyase.
P. B. Woiczikowski (2011)
Molecular origin of time-dependent fluorescence shifts in proteins.
L. Nilsson (2005)
Formation of Glasses from Liquids and Biopolymers
C. Angell (1995)
Thermodynamic and kinetic aspect
Long-range electron transfer.
H. Gray (2005)
The water flooding approach
S. Chakrabarty (2013)
Effects of solvent and solute polarizability on the reorganization energy of electron transfer
Shikha Gupta (2004)
Metalloproteins Containing Cytochrome, Iron–Sulfur, or Copper Redox Centers
J. Liu (2014)
Understanding the mechanism of short-range electron transfer using an immobilized cupredoxin.
S. Monari (2012)
Relation between charge transfer absorption and fluorescence spectra and the inverted region
R. Marcus (1989)
Electron transfer : from isolated molecules to biomolecules
M. Bixon (2007)
Communication: Microsecond dynamics of the protein and water affect electron transfer in a bacterial bc(1) complex.
D. Martin (2015)
The empirical valence
Linear response and electron transfer in complex biomolecular systems and a reaction center protein
F. Sterpone (2003)
Electron Transfer in Chemistry and Biology: An Introduction to the Theory
A. Kuznetsov (1999)
Where Is the Electronic Oscillator Strength? Mapping Oscillator Strength across Molecular Absorption Spectra.
Lianjun Zheng (2016)
The empirical valence bond model: theory and applications
Shina Caroline Lynn Kamerlin (2011)
Structural, functional and mechanistic considerations
K. Linke (2014)
The reversible opening of water channels in cytochrome c modulates the heme iron reduction potential.
C. A. Bortolotti (2012)
Theory and Applications
P. Bahr (2009)
Non-Gaussian lineshapes and dynamics of time-resolved linear and nonlinear (correlation) spectra.
M. Dinpajooh (2014)
Electrostatics and dynamics of proteins
T. Simonson (2003)
Stark effect spectroscopy of Rhodobacter sphaeroides and Rhodopseudomonas viridis reaction centers.
D. Lockhart (1988)
TOPICAL REVIEW: Violation of the fluctuation dissipation theorem in glassy systems: basic notions and the numerical evidence
A. Crisanti (2002)
Progress and challenges in simulating and understanding electron transfer in proteins.
A. de la Lande (2015)
Analysis by modern rate theory and computer simulations
M. Garcia-Viloca (2004)
Reorganization free energies for long-range electron transfer in a porphyrin-binding four-helix bundle protein.
J. Blumberger (2006)
Stark effect (electroabsorption) spectroscopy of photosynthetic reaction centers at 1.5K: Evidence that the special pair has a large excited-state polarizability
Thomas R. Middendorf (1993)
Photophysics of photosynthesis
A J Hoff (1997)
Supercooled liquids and the glass transition
P. Debenedetti (2001)
On the electron transfer mechanism
Tunneling pathway and redox-state-dependent electronic couplings at nearly fixed distance in electron transfer proteins
D. Beratan (1992)
Solvent and solute polarizability effects on the reorganization energy of electron transfer
S Gupta (2004)
Protein electron transfer: is biology (thermo)dynamic?
D. Matyushov (2015)
How Enzymes Work: Analysis by Modern Rate Theory and Computer Simulations
Mireia Garcia-Viloca (2004)
Diversity of solvent dependent energy transfer pathways in heme proteins.
Y. Zhang (2009)
Supercooled Liquids and Glass Transitions
A. Sjolander (1988)
Evidence of protein collective motions on the picosecond timescale.
Y. He (2011)
Water in Photosystem II: structural, functional and mechanistic considerations.
K. Linke (2014)
Recent Advances in the Theory and Molecular Simulation of Biological Electron Transfer Reactions.
J. Blumberger (2015)
Thermodynamic and kinetic aspects of the electron transfer reaction of bovine cytochrome c immobilized on 4-mercaptopyridine and 11-mercapto-1-undecanoic acid films
S. Monari (2008)
is biology (thermo)dynamic? J
Prediction of reorganization free energies for biological electron transfer: a comparative study of Ru-modified cytochromes and a 4-helix bundle protein.
Varomyalin Tipmanee (2010)
Thermodynamic and kinetic aspect of electron transfer reaction of bovide cytochrome c immobilized on 4-mercaptopyridine and 11-mercapto-1-undecanoid acid films
S Monari (2008)
An empirical valence bond approach for comparing reactions in solutions and in enzymes
A. Warshel (1980)
Energetics and kinetics of primary charge separation in bacterial photosynthesis.
David N. LeBard (2008)
Capturing the energetics of water insertion in biological systems: The water flooding approach
Suman Chakrabarty (2013)
Gaussian fluctuations and linear response in an electron transfer protein
T. Simonson (2002)
Energetics of Photoinduced Charge Migration within the Tryptophan Tetrad of an Animal (6-4) Photolyase.
F. Cailliez (2016)
Electron tunneling in respiratory complex I
Tomoyuki Hayashi (2010)
Scalable molecular dynamics with NAMD
J. C. Phillips (2005)
Microsecond dynamics of the protein and water affect electron transfer in a bacterial bc1 complex
D. R. Martin (2015)
The Reorganization Energy of Cytochrome c Revisited
I. Muegge (1997)
L. Kováč (2008)
Photophysics of photosynthesis. Structure and spectroscopy of reaction centers of purple bacteria
A. J. Hoff (1997)
The role of protein dynamics and thermal fluctuations in regulating cytochrome c/cytochrome c oxidase electron transfer.
Damián Alvarez-Paggi (2014)
Quantum mechanical methods for enzyme kinetics.
J. Gao (2002)
QM/MM methods for biomolecular systems.
H. Senn (2009)
Violation of the fluctuationdissipation theorem in glassy systems : basic notions and the numerical evidence
A. Crisanti (2003)
On the electron transfer mechanism between cytochrome C and metal electrodes. Evidence for dynamic control at short distances.
Hongjun Yue (2006)
Unraveling the role of the protein environment for [FeFe]-hydrogenase: a new application of coarse-graining.
Martin McCullagh (2013)
Electron transfers in chemistry and biology
R. Marcus (1985)
Understanding the Mechanism
E. Mascha (2013)
Biological charge transfer via flickering resonance
Y. Zhang (2014)
Electrostatic basis for enzyme catalysis.
A. Warshel (2006)
A hybrid approach to simulation of electron transfer in complex molecular systems
T. Kubař (2013)
This paper is referenced by
Electron-transfer chain in respiratory complex I
D. Martin (2017)
Theory and Electrochemistry of Cytochrome c.
Salman S Seyedi (2017)
Ergodicity-Breaking in Thermal Biological Electron Transfer? Cytochrome C Revisited.
Xiuyun Jiang (2019)
Dipolar susceptibility of protein hydration shells
Salman S Seyedi (2018)
Introducing the mean field approximation to CDFT/MMpol method: Statistically converged equilibrium and nonequilibrium free energy calculation for electron transfer reactions in condensed phases.
H. Nakano (2017)
Ergodicity breaking of iron displacement in heme proteins.
Salman S Seyedi (2017)