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

Abstract

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.

Authors:
 [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)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1132327
Report Number(s):
SLAC-REPRINT-2014-127
Journal ID: ISSN 0027-8424
Grant/Contract Number:  
AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 109; Journal Issue: 43; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; cytochrome oxidase; invisible states; paramagnetic proteins; NMR; spectroscopy

Citation Formats

Abriata, Luciano A., Alvarez-Paggi, Damian, Ledesma, Gabirela N., Blackburn, Ninian J., Vila, Alejandro J., and Murgida, Daniel H. Alternative ground states enable pathway switching in biological electron transfer. United States: N. p., 2012. Web. doi:10.1073/pnas.1204251109.
Abriata, Luciano A., Alvarez-Paggi, Damian, Ledesma, Gabirela N., Blackburn, Ninian J., Vila, Alejandro J., & Murgida, Daniel H. Alternative ground states enable pathway switching in biological electron transfer. United States. doi:10.1073/pnas.1204251109.
Abriata, Luciano A., Alvarez-Paggi, Damian, Ledesma, Gabirela N., Blackburn, Ninian J., Vila, Alejandro J., and Murgida, Daniel H. Wed . "Alternative ground states enable pathway switching in biological electron transfer". United States. doi:10.1073/pnas.1204251109. https://www.osti.gov/servlets/purl/1132327.
@article{osti_1132327,
title = {Alternative ground states enable pathway switching in biological electron transfer},
author = {Abriata, Luciano A. and Alvarez-Paggi, Damian and Ledesma, Gabirela N. and Blackburn, Ninian J. and Vila, Alejandro J. and Murgida, Daniel H.},
abstractNote = {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.},
doi = {10.1073/pnas.1204251109},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 43,
volume = 109,
place = {United States},
year = {2012},
month = {10}
}

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Cited by: 17 works
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