Cited by 63Metalloenzymes and iron-sulfur proteinsMitochondrial Function and PathologyProtein Structure and Dynamics

Electron-transfer chain in respiratory complex I

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Martin, Daniel R., Matyushov, Dmitry V.·2017·Scientific Reports

Abstract

Complex I is a part of the respiration energy chain converting the redox energy into the cross-membrane proton gradient. The electron-transfer chain of iron-sulfur cofactors within the water-soluble peripheral part of the complex is responsible for the delivery of electrons to the proton pumping subunit. The protein is porous to water penetration and the hydration level of the cofactors changes when the electron is transferred along the chain. High reaction barriers and trapping of the electrons at the iron-sulfur cofactors are prevented by the combination of intense electrostatic noise produced by the protein-water interface with the high density of quantum states in the iron-sulfur clusters caused by spin interactions between paramagnetic iron atoms. The combination of these factors substantially lowers the activation barrier for electron transfer compared to the prediction of the Marcus theory, bringing the rate to the experimentally established range. The unique role of iron-sulfur clusters as electron-transfer cofactors is in merging protein-water fluctuations with quantum-state multiplicity to allow low activation barriers and robust operation. Water plays a vital role in electron transport energetics by electrowetting the cofactors in the chain upon arrival of the electron. A general property of a protein is to violate the fluctuation-dissipation relation through nonergodic sampling of its landscape. High functional efficiency of redox enzymes is a direct consequence of nonergodicity.

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  1. [2]Nicholls, D. G. & Ferguson, S. J. Bioenergetics 3 (Academic Press, London, 2002).
  2. [44]Eyring, H., Lin, S. H. & Lin, S. M. Basic Chemical Kinetics (Wiley-Interscience, New York, 1980).

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Authors
Martin, D. R., & Matyushov, D. V.
Affiliations
Arizona State University (US)
Corresponding author
Matyushov, Dmitry V.
Venue
Scientific Reports
Published
2017-07-14
Volume
7
Issue
1
Pages
5495-5495
ISSN
2045-2322 (ISSN-L)
OpenAlex
W2735568116
Cited by
63
References
67
Citations by year
2026: 11 · 2025: 4 · 2024: 7 · 2023: 3 · 2022: 6 · 2021: 8 · 2020: 7 · 2019: 4 · 2018: 12 · 2017: 1
FWCI
1.76
Type
journal article
Language
en
Open access
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Arizona State University Library Digital Repository (Arizona State University) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Science Foundation (TG-MCB080116N, 1464810)
  • Division of Chemistry (CHE-1464810)
Topics
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
Keywords
mitochondrial complex I, electron transport chain, iron-sulfur clusters, protein-water interface, spin interactions, quantum states, electrowetting, ergodicity breaking, fluctuation-dissipation theorem, proton gradient, oxidative enzymes, Marcus theory
MeSH terms
Electron Transport, Thermodynamics, Time Factors, Water, Electron Transport Complex I, Molecular Dynamics Simulation

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