skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Voltage-induced long-range coherent electron transfer through organic molecules

Abstract

Biological structures rely on kinetically tuned charge transfer reactions for energy conversion, biocatalysis, and signaling as well as for oxidative damage repair. Unlike man-made electrical circuitry, which uses metals and semiconductors to direct current flow, charge transfer in living systems proceeds via biomolecules that are nominally insulating. Long-distance charge transport, which is observed routinely in nucleic acids, peptides, and proteins, is believed to arise from a sequence of thermally activated hopping steps. However, a growing number of experiments find limited temperature dependence for electron transfer over tens of nanometers. To account for these observations, we propose a temperature-independent mechanism based on the electric potential difference that builds up along the molecule as a precursor of electron transfer. Specifically, the voltage changes the nature of the electronic states away from being sharply localized so that efficient resonant tunneling across long distances becomes possible without thermal assistance. This mechanism is general and is expected to be operative in molecules where the electronic states densely fill a wide energy window (on the scale of electronvolts) above or below the gap between the highest-occupied molecular orbital (HOMO) and the lowest unoccupied molecular orbital (LUMO). We show that this effect can explain the temperature-independent chargemore » transport through DNA and the strongly voltage-dependent currents that are measured through organic semiconductors and peptides.« less

Authors:
; ; ;
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1498587
Grant/Contract Number:  
ER46430; SC0010662-ER46952
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 13; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Michaeli, Karen, Beratan, David N., Waldeck, David H., and Naaman, Ron. Voltage-induced long-range coherent electron transfer through organic molecules. United States: N. p., 2019. Web. doi:10.1073/pnas.1816956116.
Michaeli, Karen, Beratan, David N., Waldeck, David H., & Naaman, Ron. Voltage-induced long-range coherent electron transfer through organic molecules. United States. doi:10.1073/pnas.1816956116.
Michaeli, Karen, Beratan, David N., Waldeck, David H., and Naaman, Ron. Thu . "Voltage-induced long-range coherent electron transfer through organic molecules". United States. doi:10.1073/pnas.1816956116.
@article{osti_1498587,
title = {Voltage-induced long-range coherent electron transfer through organic molecules},
author = {Michaeli, Karen and Beratan, David N. and Waldeck, David H. and Naaman, Ron},
abstractNote = {Biological structures rely on kinetically tuned charge transfer reactions for energy conversion, biocatalysis, and signaling as well as for oxidative damage repair. Unlike man-made electrical circuitry, which uses metals and semiconductors to direct current flow, charge transfer in living systems proceeds via biomolecules that are nominally insulating. Long-distance charge transport, which is observed routinely in nucleic acids, peptides, and proteins, is believed to arise from a sequence of thermally activated hopping steps. However, a growing number of experiments find limited temperature dependence for electron transfer over tens of nanometers. To account for these observations, we propose a temperature-independent mechanism based on the electric potential difference that builds up along the molecule as a precursor of electron transfer. Specifically, the voltage changes the nature of the electronic states away from being sharply localized so that efficient resonant tunneling across long distances becomes possible without thermal assistance. This mechanism is general and is expected to be operative in molecules where the electronic states densely fill a wide energy window (on the scale of electronvolts) above or below the gap between the highest-occupied molecular orbital (HOMO) and the lowest unoccupied molecular orbital (LUMO). We show that this effect can explain the temperature-independent charge transport through DNA and the strongly voltage-dependent currents that are measured through organic semiconductors and peptides.},
doi = {10.1073/pnas.1816956116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 13,
volume = 116,
place = {United States},
year = {2019},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1816956116

Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Photoinduced electron transfer in supramolecular systems for artificial photosynthesis
journal, May 1992

  • Wasielewski, Michael R.
  • Chemical Reviews, Vol. 92, Issue 3, p. 435-461
  • DOI: 10.1021/cr00011a005

Direct Conductance Measurement of Single DNA Molecules in Aqueous Solution
journal, June 2004


Electron transfers in chemistry and biology
journal, August 1985

  • Marcus, R. A.; Sutin, Norman
  • Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, Vol. 811, Issue 3
  • DOI: 10.1016/0304-4173(85)90014-X

Anderson localization and delocalization in an electric field
journal, January 1986


Localization in One-Dimensional Disordered Systems in the Presence of an Electric Field
journal, March 1983


Electrostatic phenomena in organic semiconductors: fundamentals and implications for photovoltaics
journal, September 2016


Protein bioelectronics: a review of what we do and do not know
journal, January 2018

  • Bostick, Christopher D.; Mukhopadhyay, Sabyasachi; Pecht, Israel
  • Reports on Progress in Physics, Vol. 81, Issue 2
  • DOI: 10.1088/1361-6633/aa85f2

Variable-Range Hopping Electron Transfer through Disordered Bridge States:  Application to DNA
journal, October 2003

  • Renger, Thomas; Marcus, R. A.
  • The Journal of Physical Chemistry A, Vol. 107, Issue 41
  • DOI: 10.1021/jp026789c

Distance Dependence of the Charge Transfer Rate for Peptide Nucleic Acid Monolayers
journal, November 2010

  • Paul, Amit; Watson, Richard M.; Wierzbinski, Emil
  • The Journal of Physical Chemistry B, Vol. 114, Issue 45
  • DOI: 10.1021/jp906910h

Electronic structure, stacking energy, partial charge, and hydrogen bonding in four periodic B-DNA models
journal, August 2014


Long-Distance Electron Transfer Through DNA
journal, June 2002


Electron tunneling through covalent and noncovalent pathways in proteins
journal, April 1987

  • Beratan, David N.; Onuchic, José Nelson; Hopfield, J. J.
  • The Journal of Chemical Physics, Vol. 86, Issue 8
  • DOI: 10.1063/1.452723

Universality and Scaling Law of Localization Length in One-Dimensional Anderson Localization
journal, June 1996

  • Ishikawa, Masato; Kondo, Jun
  • Journal of the Physical Society of Japan, Vol. 65, Issue 6
  • DOI: 10.1143/JPSJ.65.1760

Localization dynamics and delocalization in a 1d disordered conductor in an external electric field
journal, May 1989


From Power-Localized to Extended States in a Class of One-Dimensional Disordered Systems
journal, June 1984


Charge Transport in Molecular Materials: An Assessment of Computational Methods
journal, June 2017


Localization distance and mean free path in one-dimensional disordered systems
journal, February 1973


Ultrafast Long-Range Charge Separation in Organic Semiconductor Photovoltaic Diodes
journal, December 2013


PNA versus DNA: Effects of Structural Fluctuations on Electronic Structure and Hole-Transport Mechanisms
journal, September 2008

  • Hatcher, Elizabeth; Balaeff, Alexander; Keinan, Shahar
  • Journal of the American Chemical Society, Vol. 130, Issue 35
  • DOI: 10.1021/ja802541e

Polarizability as a Molecular Descriptor for Conductance in Organic Molecular Circuits
journal, November 2016

  • Mazinani, Shobeir K. S.; Meidanshahi, Reza Vatan; Palma, Julio L.
  • The Journal of Physical Chemistry C, Vol. 120, Issue 45
  • DOI: 10.1021/acs.jpcc.6b06241

Variable-Temperature Measurements of the Single-Molecule Conductance of Double-Stranded DNA
journal, August 2006

  • van Zalinge, Harm; Schiffrin, David J.; Bates, Andrew D.
  • Angewandte Chemie International Edition, Vol. 45, Issue 33
  • DOI: 10.1002/anie.200601263

Inverse square-root field dependence of conductivity in organic field-effect transistors
journal, February 2009

  • Wei, J. H.; Gao, Y. L.; Wang, X. R.
  • Applied Physics Letters, Vol. 94, Issue 7
  • DOI: 10.1063/1.3083549

Localization in one-dimensional disordered systems with electric field: An analytical approach
journal, August 1987


Why Are DNA and Protein Electron Transfer So Different?
journal, June 2019


Engineering nanometre-scale coherence in soft matter
journal, June 2016

  • Liu, Chaoren; Xiang, Limin; Zhang, Yuqi
  • Nature Chemistry, Vol. 8, Issue 10
  • DOI: 10.1038/nchem.2545

The hole transfer in DNA: calculation of electron coupling between close bases
journal, August 2001


Recent Advances in the Theory and Molecular Simulation of Biological Electron Transfer Reactions
journal, September 2015


A Simple Index for Characterizing Charge Transport in Molecular Materials
journal, March 2015

  • Jackson, Nicholas E.; Savoie, Brett M.; Chen, Lin X.
  • The Journal of Physical Chemistry Letters, Vol. 6, Issue 6
  • DOI: 10.1021/acs.jpclett.5b00135

Protein electron transfer rates set by the bridging secondary and tertiary structure
journal, May 1991


What Controls the Rate of Ultrafast Charge Transfer and Charge Separation Efficiency in Organic Photovoltaic Blends
journal, September 2016

  • Jakowetz, Andreas C.; Böhm, Marcus L.; Zhang, Jiangbin
  • Journal of the American Chemical Society, Vol. 138, Issue 36
  • DOI: 10.1021/jacs.6b05131

Dynamically Controlled Protein Tunneling Paths in Photosynthetic Reaction Centers
journal, October 2000


Solid-State Electron Transport across Azurin: From a Temperature-Independent to a Temperature-Activated Mechanism
journal, March 2011

  • Sepunaru, Lior; Pecht, Israel; Sheves, Mordechai
  • Journal of the American Chemical Society, Vol. 133, Issue 8
  • DOI: 10.1021/ja109989f

Transport in organic semiconductors in large electric fields: From thermal activation to field emission
journal, February 2010

  • Worne, J. H.; Anthony, J. E.; Natelson, D.
  • Applied Physics Letters, Vol. 96, Issue 5
  • DOI: 10.1063/1.3309704

Density functional MO calculation for stacked DNA base-pairs with backbones
journal, May 2000


Conductance fluctuations and distribution at the metal-insulator transition induced by an electric field in a disordered chain
journal, December 2002


Dielectric functions of DNA base films from near-infrared to ultra-violet
journal, December 2005

  • Silaghi, S. D.; Friedrich, M.; Cobet, C.
  • physica status solidi (b), Vol. 242, Issue 15
  • DOI: 10.1002/pssb.200562220

Comment on “Voltage-Induced Metal-Insulator Transition in Polythiophene Field-Effect Transistors”
journal, June 2007


Solvent Fluctuations Drive the Hole Transfer in DNA: A Mixed Quantum−Classical Study
journal, October 2009

  • Kubař, Tomáš; Kleinekathöfer, Ulrich; Elstner, Marcus
  • The Journal of Physical Chemistry B, Vol. 113, Issue 39
  • DOI: 10.1021/jp9073587

Charge Transfer in Dynamical Biosystems, or The Treachery of (Static) Images
journal, October 2014

  • Beratan, David N.; Liu, Chaoren; Migliore, Agostino
  • Accounts of Chemical Research, Vol. 48, Issue 2
  • DOI: 10.1021/ar500271d

Electronic Coupling for Charge Transfer and Transport in DNA
journal, October 2000

  • Voityuk, Alexander A.; Rösch, Notker; Bixon, M.
  • The Journal of Physical Chemistry B, Vol. 104, Issue 41
  • DOI: 10.1021/jp001109w

Computational design of donor-bridge-acceptor systems exhibiting pronounced quantum interference effects
journal, January 2016

  • Gorczak, Natalie; Renaud, Nicolas; Galan, Elena
  • Physical Chemistry Chemical Physics, Vol. 18, Issue 9
  • DOI: 10.1039/C5CP06728F

Structure Controlled Long-Range Sequential Tunneling in Carbon-Based Molecular Junctions
journal, March 2017


Activationless charge transport across 4.5 to 22 nm in molecular electronic junctions
journal, March 2013

  • Yan, H.; Bergren, A. J.; McCreery, R.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 14
  • DOI: 10.1073/pnas.1221643110

Fluctuations in Biological and Bioinspired Electron-Transfer Reactions
journal, March 2010


Generalized Formula for the Electric Tunnel Effect between Similar Electrodes Separated by a Thin Insulating Film
journal, June 1963

  • Simmons, John G.
  • Journal of Applied Physics, Vol. 34, Issue 6
  • DOI: 10.1063/1.1702682

Voltage-Induced Metal-Insulator Transition in Polythiophene Field-Effect Transistors
journal, June 2006


Electric-field-dependent average resistance and the resistance fluctuation in one-dimensional disordered systems
journal, February 1987


Biological charge transfer via flickering resonance
journal, June 2014

  • Zhang, Y.; Liu, C.; Balaeff, A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 28
  • DOI: 10.1073/pnas.1316519111

Electronic Transport via Homopeptides: The Role of Side Chains and Secondary Structure
journal, July 2015

  • Sepunaru, Lior; Refaely-Abramson, Sivan; Lovrinčić, Robert
  • Journal of the American Chemical Society, Vol. 137, Issue 30
  • DOI: 10.1021/jacs.5b03933

Molecular Conductance of Nicked Nucleic Acid Duplexes
journal, February 2018

  • Beall, Edward; Sargun, Artur; Ulku, Selma
  • The Journal of Physical Chemistry C, Vol. 122, Issue 13
  • DOI: 10.1021/acs.jpcc.8b00650