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Proton-coupled electron transfer dynamics in the alternative oxidase
Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.ORCID iD: 0000-0003-2575-9913
Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics. Department of Biochemistry and Biophysics, Stockholm University, Stockholm 10691 Sweden.ORCID iD: 0000-0002-2964-5908
Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.ORCID iD: 0009-0000-8536-808X
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Number of Authors: 62024 (English)In: Chemical Science, ISSN 2041-6520, E-ISSN 2041-6539, Vol. 15, no 44, p. 18572-18580Article in journal (Refereed) Published
Abstract [en]

The alternative oxidase (AOX) is a membrane-bound di-iron enzyme that catalyzes O2-driven quinol oxidation in the respiratory chains of plants, fungi, and several pathogenic protists of biomedical and industrial interest. Yet, despite significant biochemical and structural efforts over the last decades, the catalytic principles of AOX remain poorly understood. We develop here multi-scale quantum and classical molecular simulations in combination with biochemical experiments to address the proton-coupled electron transfer (PCET) reactions responsible for catalysis in AOX from Trypanosoma brucei, the causative agent of sleeping sickness. We show that AOX activates and splits dioxygen via a water-mediated PCET reaction, resulting in a high-valent ferryl/ferric species and tyrosyl radical (Tyr220˙) that drives the oxidation of the quinol via electric field effects. We identify conserved carboxylates (Glu215, Asp100) within a buried cluster of ion-pairs that act as a transient proton-loading site in the quinol oxidation process, and validate their function experimentally with point mutations that result in drastic activity reduction and pKa-shifts. Our findings provide a key mechanistic understanding of the catalytic machinery of AOX, as well as a molecular basis for rational drug design against energy transduction chains of parasites. On a general level, our findings illustrate how redox-triggered conformational changes in ion-paired networks control the catalysis via electric field effects.

Place, publisher, year, edition, pages
2024. Vol. 15, no 44, p. 18572-18580
National Category
Biochemistry
Identifiers
URN: urn:nbn:se:su:diva-238868DOI: 10.1039/d4sc05060fISI: 001336749200001Scopus ID: 2-s2.0-85207242877OAI: oai:DiVA.org:su-238868DiVA, id: diva2:1935013
Available from: 2025-02-05 Created: 2025-02-05 Last updated: 2025-08-04Bibliographically approved
In thesis
1. Exploring Energy Conversion Mechanisms in Respiratory Enzymes
Open this publication in new window or tab >>Exploring Energy Conversion Mechanisms in Respiratory Enzymes
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

All life fundamentally relies on the efficient capture and conversion of energy into forms that support vital biochemical processes. Central to this process is the respiratory chain, a set of membrane-bound protein complexes that harness energy-rich molecules to drive ion translocation across biological membranes. This process generates an electrochemical gradient, known as the proton motive force (pmf) or sodium motive force (smf), that in turn powers the synthesis of ATP, the universal energy currency of the cell. In this thesis, the mechanistic principles underlying the function of respiratory enzymes are explored using a combination of classical molecular dynamics simulations, quantum mechanical methods, and hybrid quantum mechanics/molecular mechanics (QM/MM) calculations.

The respiratory Complex I couples the oxidation of NADH and the reduction of quinone to the translocation of four protons across biological membranes. Our results indicate that this coupling is mediated by a network of charged residues. Switching within this network triggers a conformational change of a key gating residue, thereby linking the redox reaction to ion translocation. Additionally, we identify proton translocation pathways through the membrane domain of Complex I, whose dynamics are governed by the conformation of conserved ion pairs. We investigate the mechanism of oxygen reduction and quinol oxidation by the alternative oxidase (AOX), and find that the diiron center forms a ferryl/ferric intermediate, which is reduced by the quinol in a highly exothermic reaction. To understand what drives supercomplex (SC) formation, we analyze their membrane interactions and observe that the association of Complex I and III2 into SCs reduces membrane strain. Finally, we examine the redox-coupled Na+ translocation mechanism of the Rnf complex and identify conformation dependent Na+ binding sites, based on which we propose a mechanism for ion transport. Together, the results presented in this thesis provide new insights into the mechanistic principles that govern membrane-bound respiratory enzymes.

Place, publisher, year, edition, pages
Stockholm: Department of Biochemistry and Biophysics, Stockholm University, 2025. p. 68
Keywords
Bioenergetics, Respiratory Enzymes, Proton Transfer, Energy Transduction, Multiscale Simulations
National Category
Biophysics Theoretical Chemistry Biochemistry
Research subject
Biochemistry
Identifiers
urn:nbn:se:su:diva-245310 (URN)978-91-8107-336-2 (ISBN)978-91-8107-337-9 (ISBN)
Public defence
2025-09-22, Hörsal 8, Hus D, Universitetsvägen 14 and online via Zoom, public link is available at the department website, Stockholm, 09:00 (English)
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Supervisors
Available from: 2025-08-28 Created: 2025-08-04 Last updated: 2026-05-11Bibliographically approved

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Saura, PatriciaKim, HyunhoKaila, Ville R. I.

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