ACS Publications. Most Trusted. Most Cited. Most Read
Ergodicity-Breaking in Thermal Biological Electron Transfer? Cytochrome C Revisited

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Phys. Chem. B 2019, 123, 35, 7588-7598
    Article

    Ergodicity-Breaking in Thermal Biological Electron Transfer? Cytochrome C Revisited
    Click to copy article linkArticle link copied!

    Other Access OptionsSupporting Information (1)

    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2019, 123, 35, 7588–7598
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jpcb.9b05253
    Published August 13, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    It was recently suggested that certain redox proteins operate in an ergodicity-breaking regime to facilitate biological electron transfer (ET). A signature for this is a large variance reorganization free energy (several electronvolts) but a significantly smaller Stokes reorganization free energy due to incomplete protein relaxation on the time scale of the ET event. Here we investigate whether this picture holds for oxidation of cytochrome c in aqueous solution, at various levels of theory including classical molecular dynamics with two additive and one electronically polarizable force field, and QM/MM calculations with the QM region treated by full electrostatic DFT embedding and by the perturbed matrix method. Sampling the protein and energy gap dynamics over more than 250 ns, we find no evidence for ergodicity-breaking effects. In particular, the inclusion of electronic polarizability of the heme group at QM/MM levels did not induce nonergodic effects, contrary to previous reports by Matyushov et al. The well-known problem of overestimation of reorganization free energies with additive force fields is cured when the protein and solvent are treated as electronically polarizable. Ergodicity-breaking effects may occur in other redox proteins, and our results suggest that long simulations, ideally on the ET time scale, with electronically polarizable force fields are required to obtain strong numerical evidence for them.

    Copyright © 2019 American Chemical Society

    Subjects

    what are subjects

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.9b05253.

    • Convergence of electronic polarizability and reorganization free energy with number of excited states used in QM(PMM)/MM calculations, and gap-energy autocorrelation functions (ACFs) and their time integrals (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai
    powered by  Scite

    This article is cited by 19 publications.

    1. Mohammad Mehdi Pirnia, Setare Mostajabi Sarhangi, Abhishek Singharoy, Dmitry V. Matyushov. Protein Medium Facilitates Electron Transfer in Photosynthetic Heliobacterial Reaction Center. The Journal of Physical Chemistry B 2024, 128 (40) , 9714-9723. https://doi.org/10.1021/acs.jpcb.4c04956
    2. Matthew J. Guberman-Pfeffer. Structural Determinants of Redox Conduction Favor Robustness over Tunability in Microbial Cytochrome Nanowires. The Journal of Physical Chemistry B 2023, 127 (32) , 7148-7161. https://doi.org/10.1021/acs.jpcb.3c02912
    3. Setare M. Sarhangi, Dmitry V. Matyushov. Anomalously Small Reorganization Energy of the Half Redox Reaction of Azurin. The Journal of Physical Chemistry B 2022, 126 (16) , 3000-3011. https://doi.org/10.1021/acs.jpcb.2c00338
    4. Eugen Hruska, Ariel Gale, Fang Liu. Bridging the Experiment-Calculation Divide: Machine Learning Corrections to Redox Potential Calculations in Implicit and Explicit Solvent Models. Journal of Chemical Theory and Computation 2022, 18 (2) , 1096-1108. https://doi.org/10.1021/acs.jctc.1c01040
    5. Mara Osswald, Benjamin P. Fingerhut. Electron Transfer-Induced Active Site Structural Relaxation in 64-Photolyase of Drosophila melanogaster. The Journal of Physical Chemistry B 2021, 125 (31) , 8690-8702. https://doi.org/10.1021/acs.jpcb.1c02951
    6. Zdenek Futera, Xiuyun Jiang, Jochen Blumberger. Ergodicity Breaking in Thermal Biological Electron Transfer? Cytochrome C Revisited II. The Journal of Physical Chemistry B 2020, 124 (16) , 3336-3342. https://doi.org/10.1021/acs.jpcb.0c01414
    7. Daniel R. Martin, Mohammadhasan Dinpajooh, Dmitry V. Matyushov. Polarizability of the Active Site in Enzymatic Catalysis: Cytochrome c. The Journal of Physical Chemistry B 2019, 123 (50) , 10691-10699. https://doi.org/10.1021/acs.jpcb.9b09236
    8. Matthew J. Guberman-Pfeffer, Caleb L. Herron. Cytochrome “nanowires” are physically limited to sub-picoamp currents that suffice for cellular respiration. Frontiers in Chemistry 2025, 13 https://doi.org/10.3389/fchem.2025.1549441
    9. Ljiljana Stojanović, Jack Coker, Samuele Giannini, Giacomo Londi, Anders S. Gertsen, Jens Wenzel Andreasen, Jun Yan, Gabriele D’Avino, David Beljonne, Jenny Nelson, Jochen Blumberger. Disorder-Induced Transition from Transient Quantum Delocalization to Charge Carrier Hopping Conduction in a Nonfullerene Acceptor Material. Physical Review X 2024, 14 (2) https://doi.org/10.1103/PhysRevX.14.021021
    10. Jan Vacek, Martina Zatloukalová, Vlastimil Dorčák, Michal Cifra, Zdeněk Futera, Veronika Ostatná. Electrochemistry in sensing of molecular interactions of proteins and their behavior in an electric field. Microchimica Acta 2023, 190 (11) https://doi.org/10.1007/s00604-023-05999-2
    11. Setare Mostajabi Sarhangi, Dmitry V. Matyushov. Comment on “Applicability of perturbed matrix method for charge transfer studies at bio/metallic interfaces: a case of azurin” by O. Kontkanen, D. Biriukov and Z. Futera, Phys. Chem. Chem. Phys. , 2023, 25 , 12479. Physical Chemistry Chemical Physics 2023, 25 (39) , 26923-26928. https://doi.org/10.1039/D3CP03178K
    12. Xiyue Bai, Pengfei Li, Wuxian Peng, Ningyue Chen, Jin‐Liang Lin, Yuan Li. Ionogel‐Electrode for the Study of Protein Tunnel Junctions under Physiologically Relevant Conditions. Advanced Materials 2023, 35 (26) https://doi.org/10.1002/adma.202300663
    13. Outi Vilhelmiina Kontkanen, Denys Biriukov, Zdenek Futera. Applicability of perturbed matrix method for charge transfer studies at bio/metallic interfaces: a case of azurin. Physical Chemistry Chemical Physics 2023, 25 (17) , 12479-12489. https://doi.org/10.1039/D3CP00197K
    14. Giulia Di Rocco, Antonio Ranieri, Marco Borsari, Marco Sola, Carlo Augusto Bortolotti, Gianantonio Battistuzzi. Assessing the Functional and Structural Stability of the Met80Ala Mutant of Cytochrome c in Dimethylsulfoxide. Molecules 2022, 27 (17) , 5630. https://doi.org/10.3390/molecules27175630
    15. Ankita Sarkar, Samir Chattopadhyay, Manjistha Mukherjee, Somdatta Ghosh Dey, Abhishek Dey. Assembly of redox active metallo-enzymes and metallo-peptides on electrodes: Abiological constructs to probe natural processes. Current Opinion in Chemical Biology 2022, 68 , 102142. https://doi.org/10.1016/j.cbpa.2022.102142
    16. Peter J. Dahl, Sophia M. Yi, Yangqi Gu, Atanu Acharya, Catharine Shipps, Jens Neu, J. Patrick O’Brien, Uriel N. Morzan, Subhajyoti Chaudhuri, Matthew J. Guberman-Pfeffer, Dennis Vu, Sibel Ebru Yalcin, Victor S. Batista, Nikhil S. Malvankar. A 300-fold conductivity increase in microbial cytochrome nanowires due to temperature-induced restructuring of hydrogen bonding networks. Science Advances 2022, 8 (19) https://doi.org/10.1126/sciadv.abm7193
    17. Outi Vilhelmiina Kontkanen, Denys Biriukov, Zdenek Futera. Reorganization free energy of copper proteins in solution, in vacuum, and on metal surfaces. The Journal of Chemical Physics 2022, 156 (17) https://doi.org/10.1063/5.0085141
    18. Eugen Hruska, Ariel Gale, Xiao Huang, Fang Liu. AutoSolvate: A toolkit for automating quantum chemistry design and discovery of solvated molecules. The Journal of Chemical Physics 2022, 156 (12) https://doi.org/10.1063/5.0084833
    19. Samir Chattopadhyay, Manjistha Mukherjee, Banu Kandemir, Sarah E. J. Bowman, Kara L. Bren, Abhishek Dey. Contributions to cytochrome c inner- and outer-sphere reorganization energy. Chemical Science 2021, 12 (35) , 11894-11913. https://doi.org/10.1039/D1SC02865K
    Download PDF
    Go to The Journal of Physical Chemistry B
    Get e-Alerts
    Get e-Alerts

    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2019, 123, 35, 7588–7598
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jpcb.9b05253
    Published August 13, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

    Article Views

    815

    Altmetric

    -

    Citations

    19
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.