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

Title: Alternative ground states enable pathway switching in biological electron transfer

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [1];  [3];  [1];  [2]
  1. Univ. Nacional de Rosario, Rosario (Argentina)
  2. Univ. de Buenos Aires, Buenos Aires (Argentina)
  3. Oregon Health and Sciences Univ., Beaverton, OR (United States)
+ Show Author Affiliations

Electron transfer is the simplest chemical reaction and constitutes the basis of a large variety of biological processes, such as photosynthesis and cellular respiration. Nature has evolved specific proteins and cofactors for these functions. The mechanisms optimizing biological electron transfer have been matter of intense debate, such as the role of the protein milieu between donor and acceptor sites. Here we propose a mechanism regulating long-range electron transfer in proteins. Specifically, we report a spectroscopic, electrochemical, and theoretical study on WT and single-mutant CuA redox centers from Thermus thermophilus, which shows that thermal fluctuations may populate two alternative ground-state electronic wave functions optimized for electron entry and exit, respectively, through two different and nearly perpendicular pathways. In conclusion, these findings suggest a unique role for alternative or “invisible” electronic ground states in directional electron transfer. Moreover, it is shown that this energy gap and, therefore, the equilibrium between ground states can be fine-tuned by minor perturbations, suggesting alternative ways through which protein–protein interactions and membrane potential may optimize and regulate electron–proton energy transduction.

Research Organization:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-76SF00515
OSTI ID:
1132327
Report Number(s):
SLAC-REPRINT-2014-127
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, Issue 43; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 29 works
Citation information provided by
Web of Science

References (38)

Spectroscopy of Mixed-Valence Cu A -Type Centers:  Ligand-Field Control of Ground-State Properties Related to Electron Transfer journal June 1998
Molecular Basis of Coupled Protein and Electron Transfer Dynamics of Cytochrome c in Biomimetic Complexes journal May 2010
The currents of life: the terminal electron-transfer complex of respiration. journal December 1995
Electron Transfer Between Biological Molecules by Thermally Activated Tunneling journal September 1974
Electron transfers in chemistry and biology journal August 1985
Geometry, Reduction Potential, and Reorganization Energy of the Binuclear Cu A Site, Studied by Density Functional Theory journal August 2001
Nature of biological electron transfer journal February 1992
Direct Observation of the Gating Step in Protein Electron Transfer: Electric-Field-Controlled Protein Dynamics journal July 2008
Internal Electron-Transfer Reactions in Cytochrome c Oxidase † journal January 1996
A Quantitative Description of the Ground-State Wave Function of Cu A by X-ray Absorption Spectroscopy:  Comparison to Plastocyanin and Relevance to Electron Transfer journal June 2001
New Tools Provide New Insights in NMR Studies of Protein Dynamics journal April 2006
Perturbations to the Geometric and Electronic Structure of the Cu A Site: Factors that Influence Delocalization and Their Contributions to Electron Transfer journal April 2008
Electron transfer among the Cu A -, heme b - and a 3 -centers of Thermus thermophilus cytochrome ba 3 journal May 2006
Probing Invisible, Low-Populated States of Protein Molecules by Relaxation Dispersion NMR Spectroscopy: An Application to Protein Folding journal March 2008
The Met Axial Ligand Determines the Redox Potential in Cu A Sites journal October 2007
Interaction-induced Redox Switch in the Electron Transfer Complex Rusticyanin-Cytochrome c 4 journal October 1999
Ab Initio Based Calculations of Electron-Transfer Rates in Metalloproteins journal February 2005
A novel cryoprotection scheme for enhancing the diffraction of crystals of recombinant cytochrome ba 3 oxidase from Thermus thermophilus journal February 2005
Effect of Electron-Transfer Rate and Reorganization Energy on the Cyclic Voltammetric Response of Redox Adsorbates journal July 1999
Persistence of Structure Over Fluctuations in Biological Electron-Transfer Reactions journal October 2008
The Two-State Issue in the Mixed-Valence Binuclear Cu A Center in Cytochrome c Oxidase and N 2 O Reductase journal December 2006
Protein electron transfer rates set by the bridging secondary and tertiary structure journal May 1991
Electronic structure contributions to electron transfer in blue Cu and CuA journal February 2000
Molecular Basis of Coupled Protein and Electron Transfer Dynamics of Cytochrome c in Biomimetic Complexes journal April 2010
Heme-protein vibrational couplings in cytochrome c provide a dynamic link that connects the heme-iron and the protein surface journal May 2012
Systematic ab initio study of the electronic and magnetic properties of different pure and mixed iron systems journal May 2000
Mapping electron tunneling pathways: an algorithm that finds the "minimum length"/maximum coupling pathway between electron donors and acceptors in proteins journal May 1992
General expression of the linear potential sweep voltammogram in the case of diffusionless electrochemical systems journal July 1979
Electronic Structure of the Ground and Excited States of the Cu A Site by NMR Spectroscopy journal February 2009
A DFT-Based QM-MM Approach Designed for the Treatment of Large Molecular Systems:  Application to Chorismate Mutase journal December 2003
The Electron Transfer Complex between Cytochrome c 552 and the Cu A Domain of the Thermus thermophilus ba 3 Oxidase : A COMBINED NMR AND COMPUTATIONAL APPROACH journal March 2006
Fluctuations in Biological and Bioinspired Electron-Transfer Reactions journal March 2010
Protein dynamics and electron transfer: Electronic decoherence and non-Condon effects journal February 2005
The Cu A Center of a Soluble Domain from Thermus Cytochrome ba 3 . An NMR Investigation of the Paramagnetic Protein journal January 1996
Transient binding of plastocyanin to its physiological redox partners modifies the copper site geometry journal October 2006
Long-range electron transfer journal February 2005
Understanding the Electronic Properties of the Cu A Site from the Soluble Domain of Cytochrome c Oxidase through Paramagnetic 1 H NMR † journal May 1998
Complex formation between methylamine dehydrogenase and amicyanin from Paracoccus denitrificans. journal October 1988

Cited By (4)

DEPC modification of the CuA protein from Thermus thermophilus journal December 2018
The role of protein dynamics and thermal fluctuations in regulating cytochrome c/cytochrome c oxidase electron transfer journal July 2014
Unexpected Electron Spin Density on the Axial Methionine Ligand in CuA Suggests Its Involvement in Electron Pathway posted_content November 2019
Unexpected electron spin density on the axial methionine ligand in Cu A suggests its involvement in electron pathways journal January 2020

Similar Records

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
cytochrome oxidase
invisible states
paramagnetic proteins
NMR
spectroscopy