Proton-Coupled Electron Transfer Drives Long-Range Proton Translocation in Bioinspired Systems

Emmanuel Odella, Brian L. Wadsworth, S. Jimena Mora, Joshua J. Goings, Mioy T. Huynh, John Devens Gust, Thomas A Moore, Gary F. Moore, Sharon Hammes-Schiffer, Ana L. Moore

Research output: Contribution to journalArticle

Abstract

Proton-coupled electron transfer (PCET) combines the movement of fundamental charged species to form an essential link between electron- and proton-transport reactions in bioenergetics and catalysis in general. The length scale over which proton transport may occur within PCET processes and the thermodynamic consequences of the resulting proton chemical potential to the oxidation reaction driving these PCET processes have not been generally established. Here we report the design of bioinspired molecules that employ oxidation-reduction processes to move reversibly two, three, and four protons via a Grotthuss-type mechanism along hydrogen-bonded networks up to ∼16 Å in length. These molecules are composed of benzimidazole moieties linking a phenol to the final proton acceptor, a cyclohexylimine. Following electrochemical oxidation of the phenol, the appearance of an infrared band at 1660 cm-1 signals proton arrival at the terminal basic site. Switching the electrode potential to reducing conditions reverses the proton translocation and resets the structure to the initial species. In addition to mimicking the first step of the iconic PCET process used by the Tyrz-His190 redox relay in photosystem II to oxidize water, this work specifically addresses theoretically and experimentally the length scale over which PCET processes may occur. The thermodynamic findings from these redox-driven, bioinspired "proton wires" have implications for understanding and rationally designing pumps for the generation of proton-motive force in artificial and reengineered photosynthesis, as well as for management of proton activity around catalytic sites, including those for water oxidation and oxygen reduction.

Original languageEnglish
JournalJournal of the American Chemical Society
DOIs
Publication statusAccepted/In press - Jan 1 2019

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Protons
Electrons
Oxidation-Reduction
Phenol
Thermodynamics
Phenols
Proton-Motive Force
Photosystem II Protein Complex
Oxidation
Water
Molecules
Photosynthesis
Electrochemical oxidation
Chemical potential
Electron Transport
Catalysis
Energy Metabolism
Hydrogen
Catalytic Domain
Electrodes

ASJC Scopus subject areas

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

Proton-Coupled Electron Transfer Drives Long-Range Proton Translocation in Bioinspired Systems. / Odella, Emmanuel; Wadsworth, Brian L.; Mora, S. Jimena; Goings, Joshua J.; Huynh, Mioy T.; Gust, John Devens; Moore, Thomas A; Moore, Gary F.; Hammes-Schiffer, Sharon; Moore, Ana L.

In: Journal of the American Chemical Society, 01.01.2019.

Research output: Contribution to journalArticle

Odella, Emmanuel ; Wadsworth, Brian L. ; Mora, S. Jimena ; Goings, Joshua J. ; Huynh, Mioy T. ; Gust, John Devens ; Moore, Thomas A ; Moore, Gary F. ; Hammes-Schiffer, Sharon ; Moore, Ana L. / Proton-Coupled Electron Transfer Drives Long-Range Proton Translocation in Bioinspired Systems. In: Journal of the American Chemical Society. 2019.
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