Electronic coupling through natural amino acids

Berstis, Laura; Beckham, Gregg T.; Crowley, Michael F.

doi:10.1063/1.4936588

Title: Electronic coupling through natural amino acids

Journal Article · Tue Dec 08 00:00:00 EST 2015 · Journal of Chemical Physics

DOI:https://doi.org/10.1063/1.4936588· OSTI ID:1235671

Berstis, Laura ^[1]; Beckham, Gregg T. ^[1];

^[1]

National Renewable Energy Lab. (NREL), Golden, CO (United States)

Myriad scientific domains concern themselves with biological electron transfer (ET) events that span across vast scales of rate and efficiency through a remarkably fine-tuned integration of amino acid (AA) sequences, electronic structure, dynamics, and environment interactions. Within this intricate scheme, many questions persist as to how proteins modulate electron-tunneling properties. To help elucidate these principles, we develop a model set of peptides representing the common α-helix and β-strand motifs including all natural AAs within implicit protein-environment solvation. Using an effective Hamiltonian strategy with density functional theory, we characterize the electronic coupling through these peptides, furthermore considering side-chain dynamics. For both motifs, predictions consistently show that backbone-mediated electronic coupling is distinctly sensitive to AA type (aliphatic, polar, aromatic, negatively charged and positively charged), and to side-chain orientation. Here, the unique properties of these residues may be employed to design activated, deactivated, or switch-like superexchange pathways. Electronic structure calculations and Green’s function analyses indicate that localized shifts in the electron density along the peptide play a role in modulating these pathways, and further substantiate the experimentally observed behavior of proline residues as superbridges.

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Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office (BETO); Swiss National Science Foundation (SNSF)

Grant/Contract Number:: AC36-08GO28308; MCB09159

OSTI ID:: 1235671

Alternate ID(s):: OSTI ID: 1228434

Report Number(s):: NREL/JA-2700-64983; JCPSA6

Journal Information:: Journal of Chemical Physics, Vol. 143, Issue 22; Related Information: Journal of Chemical Physics; ISSN 0021-9606

Publisher:: American Institute of Physics (AIP)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 11 works

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References (69)

Study of long-range .pi.,.pi. interactions in rigid molecules by electron transmission spectroscopy Balaji, V.; Ng, L.; Jordan, K. D. Journal of the American Chemical Society, Vol. 109, Issue 23 https://doi.org/10.1021/ja00257a010	journal	November 1987
Tryptophan-Accelerated Electron Flow Through Proteins Shih, C.; Museth, A. K.; Abrahamsson, M. Science, Vol. 320, Issue 5884 https://doi.org/10.1126/science.1158241	journal	June 2008
Outlying Charge, Stability, Efficiency, and Algorithmic Enhancements in the Quantum-Mechanical Solvation Method, COSab-GAMESS Gregerson, Laura N.; Baldridge, Kim K. Helvetica Chimica Acta, Vol. 86, Issue 12 https://doi.org/10.1002/hlca.200390340	journal	December 2003
Quantum tunneling in biological reactions: the interplay between theory and experiments Onuchic, José N.; Kobayashi, Chigusa; Baldridge, Kim K. Journal of the Brazilian Chemical Society, Vol. 19, Issue 2 https://doi.org/10.1590/S0103-50532008000200003	journal	January 2008
Quantum mechanical calculations suggest that lytic polysaccharide monooxygenases use a copper-oxyl, oxygen-rebound mechanism Kim, S.; Stahlberg, J.; Sandgren, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1316609111	journal	December 2013
Electron transfers in chemistry and biology Marcus, R. A.; Sutin, Norman Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, Vol. 811, Issue 3 https://doi.org/10.1016/0304-4173(85)90014-X	journal	August 1985
Stabilization of Non-productive Conformations Underpins Rapid Electron Transfer to Electron-transferring Flavoprotein Toogood, Helen S.; van Thiel, Adam; Scrutton, Nigel S. Journal of Biological Chemistry, Vol. 280, Issue 34 https://doi.org/10.1074/jbc.M505562200	journal	June 2005
Electron flow in multiheme bacterial cytochromes is a balancing act between heme electronic interaction and redox potentials Breuer, M.; Rosso, K. M.; Blumberger, J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 2 https://doi.org/10.1073/pnas.1316156111	journal	January 2014
Charge Transfer in E. coli DNA Photolyase: Understanding Polarization and Stabilization Effects via QM/MM Simulations Lüdemann, Gesa; Woiczikowski, P. Benjamin; Kubař, Tomáš The Journal of Physical Chemistry B, Vol. 117, Issue 37 https://doi.org/10.1021/jp406319b	journal	September 2013
Electron transfer in human cytochrome P450 reductase Gutierrez, A.; Grunau, A.; Paine, M. Biochemical Society Transactions, Vol. 31, Issue 3 https://doi.org/10.1042/bst0310497	journal	June 2003
Electron Relay Race in Peptides Giese, Bernd; Wang, Min; Gao, Jian The Journal of Organic Chemistry, Vol. 74, Issue 10 https://doi.org/10.1021/jo900375f	journal	May 2009
Electronic couplings for molecular charge transfer: Benchmarking CDFT, FODFT, and FODFTB against high-level ab initio calculations Kubas, Adam; Hoffmann, Felix; Heck, Alexander The Journal of Chemical Physics, Vol. 140, Issue 10 https://doi.org/10.1063/1.4867077	journal	March 2014
Electron transfer in azurin and the role of aromatic side groups of the protein Broo, A.; Larsson, S. The Journal of Physical Chemistry, Vol. 95, Issue 13 https://doi.org/10.1021/j100166a002	journal	June 1991
Does π−σ−π Through-Bond Coupling Significantly Increase C−C Bond Lengths? Battersby, Thomas R.; VernonClark, Russell; Siegel, Jay S. Journal of the American Chemical Society, Vol. 119, Issue 30 https://doi.org/10.1021/ja9622315	journal	July 1997
Coupling Coherence Distinguishes Structure Sensitivity in Protein Electron Transfer Prytkova, T. R.; Kurnikov, I. V.; Beratan, D. N. Science, Vol. 315, Issue 5812 https://doi.org/10.1126/science.1134862	journal	February 2007
Donor/Acceptor Coupling Shortcuts in Electron Transfer within Ruthenium-Modified Derivatives of Cytochrome b ₅₆₂ Prytkova, Tatiana R.; Shunaev, Vladislav V.; Glukhova, Olga E. The Journal of Physical Chemistry B, Vol. 119, Issue 4 https://doi.org/10.1021/jp5086894	journal	January 2015
Mechanism for electron transfer within and between proteins Page, C. Current Opinion in Chemical Biology, Vol. 7, Issue 5 https://doi.org/10.1016/j.cbpa.2003.08.005	journal	October 2003
Electron transfer in peptides Shah, Afzal; Adhikari, Bimalendu; Martic, Sanela Chemical Society Reviews, Vol. 44, Issue 4 https://doi.org/10.1039/C4CS00297K	journal	January 2015
Solar hydrogen-producing bionanodevice outperforms natural photosynthesis Lubner, C. E.; Applegate, A. M.; Knorzer, P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 52 https://doi.org/10.1073/pnas.1114660108	journal	December 2011
A predictive theoretical model for electron tunneling pathways in proteins Onuchic, José Nelson; Beratan, David N. The Journal of Chemical Physics, Vol. 92, Issue 1 https://doi.org/10.1063/1.458426	journal	January 1990
Extracting electron transfer coupling elements from constrained density functional theory Wu, Qin; Van Voorhis, Troy The Journal of Chemical Physics, Vol. 125, Issue 16 https://doi.org/10.1063/1.2360263	journal	October 2006
Long-Range Electron Transfer Across Peptide Bridges: The Transition from Electron Superexchange to Hopping Malak, Rouba Abdel; Gao, Zhinong; Wishart, James F. Journal of the American Chemical Society, Vol. 126, Issue 43 https://doi.org/10.1021/ja0401040	journal	November 2004
Analysis of Main Chain Torsion Angles in Proteins: Prediction of NMR Coupling Constants for Native and Random Coil Conformations Smith, Lorna J.; Bolin, Kimberly A.; Schwalbe, Harald Journal of Molecular Biology, Vol. 255, Issue 3 https://doi.org/10.1006/jmbi.1996.0041	journal	January 1996
Electron-Transfer Mechanisms through Biological Redox Chains in Multicenter Enzymes Jeuken, Lars J. C.; Jones, Anne K.; Chapman, Stephen K. Journal of the American Chemical Society, Vol. 124, Issue 20 https://doi.org/10.1021/ja012638w	journal	May 2002
Accessibility, Reactivity, and Selectivity of Side Chains within a Channel of de Novo Peptide Assembly Burton, Antony J.; Thomas, Franziska; Agnew, Christopher Journal of the American Chemical Society, Vol. 135, Issue 34 https://doi.org/10.1021/ja4053027	journal	August 2013
Primary structure effects on peptide group hydrogen exchange Bai, Yawen; Milne, John S.; Mayne, Leland Proteins: Structure, Function, and Genetics, Vol. 17, Issue 1 https://doi.org/10.1002/prot.340170110	journal	September 1993
Influence of Amino Acid Side Chains on Long-Distance Electron Transfer in Peptides: Electron Hopping via “Stepping Stones” Cordes, Meike; Köttgen, Angnieszka; Jasper, Christian Angewandte Chemie International Edition, Vol. 47, Issue 18 https://doi.org/10.1002/anie.200705588	journal	April 2008
Electron transfer in ruthenium-modified proteins Bjerrum, Morten J.; Casimiro, Danilo R.; Chang, I. -Jy. Journal of Bioenergetics and Biomembranes, Vol. 27, Issue 3 https://doi.org/10.1007/BF02110099	journal	June 1995
Dynamics driving function − new insights from electron transferring flavoproteins and partner complexes: ETF and partners - structure, function and dynamics Toogood, Helen S.; Leys, David; Scrutton, Nigel S. FEBS Journal, Vol. 274, Issue 21 https://doi.org/10.1111/j.1742-4658.2007.06107.x	journal	October 2007
Fragment Orbital Based Description of Charge Transfer in Peptides Including Backbone Orbitals Heck, Alexander; Woiczikowski, P. Benjamin; Kubař, Tomáš The Journal of Physical Chemistry B, Vol. 118, Issue 16 https://doi.org/10.1021/jp408907g	journal	April 2014
Nearest-neighbor effects and structural preferences in dipeptides are a function of the electronic properties of amino acid side-chains Dwyer, Donard S. Proteins: Structure, Function, and Bioinformatics, Vol. 63, Issue 4 https://doi.org/10.1002/prot.20906	journal	February 2006
Molecular structure and free energy landscape for electron transport in the decahaem cytochrome MtrF Breuer, Marian; Zarzycki, Piotr; Shi, Liang Biochemical Society Transactions, Vol. 40, Issue 6 https://doi.org/10.1042/BST20120139	journal	November 2012
Electron transfer in peptides and proteins Giese, Bernd; Graber, Michael; Cordes, Meike Current Opinion in Chemical Biology, Vol. 12, Issue 6 https://doi.org/10.1016/j.cbpa.2008.08.026	journal	December 2008
Through-Bond Orbital Coupling, the Parity Rule, and the Design of “Superbridges” Which Exhibit Greatly Enhanced Electronic Coupling: A Natural Bond Orbital Analysis Paddon-Row, Michael N.; Shephard, Michael J. Journal of the American Chemical Society, Vol. 119, Issue 23 https://doi.org/10.1021/ja964132x	journal	June 1997
β-Hairpin Peptidomimetics: Design, Structures and Biological Activities Robinson, John A. Accounts of Chemical Research, Vol. 41, Issue 10 https://doi.org/10.1021/ar700259k	journal	October 2008
Long Distance Electron-Transfer Mechanism in Peptidylglycine α-Hydroxylating Monooxygenase: A Perfect Fitting for a Water Bridge de la Lande, Aurélien; Martí, Sergio; Parisel, Olivier Journal of the American Chemical Society, Vol. 129, Issue 38 https://doi.org/10.1021/ja070329l	journal	September 2007
Distance Dependence of Electron Transfer Across Peptides with Different Secondary Structures: The Role of Peptide Energetics and Electronic Coupling Shin, Yeung-gyo K.; Newton, Marshall D.; Isied, Stephan S. Journal of the American Chemical Society, Vol. 125, Issue 13 https://doi.org/10.1021/ja020358q	journal	April 2003
Ultrafast Estimation of Electronic Couplings for Electron Transfer between π-Conjugated Organic Molecules Gajdos, Fruzsina; Valner, Siim; Hoffmann, Felix Journal of Chemical Theory and Computation, Vol. 10, Issue 10 https://doi.org/10.1021/ct500527v	journal	September 2014
Development of a Model System for the Study of Long Distance Electron Transfer in Peptides Cordes, Meike; Jacques, Olivier; Köttgen, Agnieszka Advanced Synthesis & Catalysis, Vol. 350, Issue 7-8 https://doi.org/10.1002/adsc.200700605	journal	May 2008
Gating mechanisms for biological electron transfer: Integrating structure with biophysics reveals the nature of redox control in cytochrome P450 reductase and copper-dependent nitrite reductase Leferink, Nicole G. H.; Pudney, Christopher R.; Brenner, Sibylle FEBS Letters, Vol. 586, Issue 5 https://doi.org/10.1016/j.febslet.2011.07.003	journal	July 2011
Erratum: “Comparative study of perturbative methods for computing electron transfer tunneling matrix elements with a nonorthogonal basis set” [J. Chem. Phys. 125, 244103 (2006)] Teklos, Antonios; Skourtis, Spiros S. The Journal of Chemical Physics, Vol. 126, Issue 20 https://doi.org/10.1063/1.2737445	journal	May 2007
Mechanisms of Long-Distance Electron Transfer in Proteins: Lessons from Photosynthetic Reaction Centers Boxer, S. G. Annual Review of Biophysics and Biophysical Chemistry, Vol. 19, Issue 1 https://doi.org/10.1146/annurev.bb.19.060190.001411	journal	June 1990
Design and engineering of photosynthetic light-harvesting and electron transfer using length, time, and energy scales Noy, Dror; Moser, Christopher C.; Dutton, P. Leslie Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 2 https://doi.org/10.1016/j.bbabio.2005.11.010	journal	February 2006
Multiple versus single pathways in electron transfer in proteins: Influence of protein dynamics and hydrogen bonds Kobayashi, Chigusa; Baldridge, Kim; Onuchic, José N. The Journal of Chemical Physics, Vol. 119, Issue 6 https://doi.org/10.1063/1.1588293	journal	August 2003
Intermolecular Electron-Transfer Reactions in Soluble Methane Monooxygenase: A Role for Hysteresis in Protein Function Blazyk, Jessica L.; Gassner, George T.; Lippard, Stephen J. Journal of the American Chemical Society, Vol. 127, Issue 49 https://doi.org/10.1021/ja0554054	journal	December 2005
General atomic and molecular electronic structure system Schmidt, Michael W.; Baldridge, Kim K.; Boatz, Jerry A. Journal of Computational Chemistry, Vol. 14, Issue 11, p. 1347-1363 https://doi.org/10.1002/jcc.540141112	journal	November 1993
Distal Charge Transport in Peptides Schlag, Edward W.; Sheu, Sheh-Yi; Yang, Dah-Yen Angewandte Chemie International Edition, Vol. 46, Issue 18 https://doi.org/10.1002/anie.200601623	journal	April 2007
Disentangling Electron Tunneling and Protein Dynamics of Cytochrome c through a Rationally Designed Surface Mutation Alvarez-Paggi, Damián; Meister, Wiebke; Kuhlmann, Uwe The Journal of Physical Chemistry B, Vol. 117, Issue 20 https://doi.org/10.1021/jp400832m	journal	May 2013
Calculation of the total electrostatic energy of a macromolecular system: Solvation energies, binding energies, and conformational analysis Gilson, Michael K.; Honig, Barry Proteins: Structure, Function, and Genetics, Vol. 4, Issue 1 https://doi.org/10.1002/prot.340040104	journal	January 1988
Structure and boosting activity of a starch-degrading lytic polysaccharide monooxygenase Lo Leggio, Leila; Simmons, Thomas J.; Poulsen, Jens-Christian N. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms6961	journal	January 2015
Protein electron transfer rates set by the bridging secondary and tertiary structure Beratan, D.; Betts, J.; Onuchic, J. Science, Vol. 252, Issue 5010 https://doi.org/10.1126/science.1656523	journal	May 1991
Bridge‐mediated electronic interactions: Differences between Hamiltonian and Green function partitioning in a non‐orthogonal basis Priyadarshy, Satyam; Skourtis, Spiros S.; Risser, Steven M. The Journal of Chemical Physics, Vol. 104, Issue 23 https://doi.org/10.1063/1.471690	journal	June 1996
Nature of the Energy Landscape for Gated Electron Transfer in a Dynamic Redox Protein Hay, Sam; Brenner, Sibylle; Khara, Basile Journal of the American Chemical Society, Vol. 132, Issue 28 https://doi.org/10.1021/ja1016206	journal	July 2010
Electron Transfer in Proteins Gray, Harry B.; Winkler, Jay R. Annual Review of Biochemistry, Vol. 65, Issue 1 https://doi.org/10.1146/annurev.bi.65.070196.002541	journal	June 1996
Probing Electron-Transfer Times in Photosynthetic Reaction Centers by Hole-Burning Spectroscopy Jankowiak, Ryszard The Journal of Physical Chemistry Letters, Vol. 3, Issue 12 https://doi.org/10.1021/jz300505r	journal	June 2012
A fast intrinsic localization procedure applicable for a b i n i t i o and semiempirical linear combination of atomic orbital wave functions Pipek, János; Mezey, Paul G. The Journal of Chemical Physics, Vol. 90, Issue 9 https://doi.org/10.1063/1.456588	journal	May 1989
Solvent Driving Force Ensures Fast Formation of a Persistent and Well-Separated Radical Pair in Plant Cryptochrome Lüdemann, Gesa; Solov’yov, Ilia A.; Kubař, Tomáš Journal of the American Chemical Society, Vol. 137, Issue 3 https://doi.org/10.1021/ja510550g	journal	January 2015
Pathway Analysis of Protein Electron-Transfer Reactions Onuchic, J. N.; Beratan, D. N.; Winkler, J. R. Annual Review of Biophysics and Biomolecular Structure, Vol. 21, Issue 1 https://doi.org/10.1146/annurev.bb.21.060192.002025	journal	June 1992
Semiempirical GGA-type density functional constructed with a long-range dispersion correction Grimme, Stefan Journal of Computational Chemistry, Vol. 27, Issue 15, p. 1787-1799 https://doi.org/10.1002/jcc.20495	journal	January 2006
Sidechain torsional potentials and motion of amino acids in porteins: bovine pancreatic trypsin inhibitor. Gelin, B. R.; Karplus, M. Proceedings of the National Academy of Sciences, Vol. 72, Issue 6 https://doi.org/10.1073/pnas.72.6.2002	journal	June 1975
Tryptophan-Accelerated Electron Flow Across a Protein–Protein Interface Takematsu, Kana; Williamson, Heather; Blanco-Rodríguez, Ana María Journal of the American Chemical Society, Vol. 135, Issue 41 https://doi.org/10.1021/ja406830d	journal	October 2013
Amplification of Single Molecule Translocation Signal Using β-Strand Peptide Functionalized Nanopores Liebes-Peer, Yael; Rapaport, Hanna; Ashkenasy, Nurit ACS Nano, Vol. 8, Issue 7 https://doi.org/10.1021/nn501331u	journal	June 2014
Electron tunneling in respiratory complex I Hayashi, T.; Stuchebrukhov, A. A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 45 https://doi.org/10.1073/pnas.1009181107	journal	October 2010
Charge Transfer in Dynamical Biosystems, or The Treachery of (Static) Images Beratan, David N.; Liu, Chaoren; Migliore, Agostino Accounts of Chemical Research, Vol. 48, Issue 2 https://doi.org/10.1021/ar500271d	journal	October 2014
XVIth International Conference on Biological Inorganic Chemistry JBIC Journal of Biological Inorganic Chemistry, Vol. 19, Issue S1, p. 1-696 https://doi.org/10.1007/s00775-014-1095-8	journal	March 2014
Fully optimized contracted Gaussian basis sets of triple zeta valence quality for atoms Li to Kr Schäfer, Ansgar; Huber, Christian; Ahlrichs, Reinhart The Journal of Chemical Physics, Vol. 100, Issue 8 https://doi.org/10.1063/1.467146	journal	April 1994
GdDO3NI, a nitroimidazole-based T 1 MRI contrast agent for imaging tumor hypoxia in vivo Gulaka, Praveen K.; Rojas-Quijano, Federico; Kovacs, Zoltan JBIC Journal of Biological Inorganic Chemistry, Vol. 19, Issue 2 https://doi.org/10.1007/s00775-013-1058-5	journal	November 2013
Correlation of electron transfer rate in photosynthetic reaction centers with intraprotein dielectric properties Chamorovsky, Sergey K.; Cherepanov, Dmitry A.; Chamorovsky, Constantin S. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 6 https://doi.org/10.1016/j.bbabio.2007.01.008	journal	June 2007
Electronic structure and bonding of the amino acids containing first row atoms. Dixon, D. A.; Lipscomb, W. N. Journal of Biological Chemistry, Vol. 251, Issue 19 https://doi.org/10.1016/S0021-9258(17)33049-1	journal	October 1976

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09 BIOMASS FUELS
59 BASIC BIOLOGICAL SCIENCES
electron transfer
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electron tunneling
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superexchange
peptide electron transfer
protein engineering
amino acid
electronic coupling
peptides
biosensors
chemical bonding
density functional theory
biological electron transfer
electronic structure methods

Title: Electronic coupling through natural amino acids

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