Photogeneration and reactivity of flavin anionic semiquinone in a bifurcating electron transfer flavoprotein

Duan, H. Diessel; Khan, Sharique A.; Miller, Anne-Frances

doi:10.1016/j.bbabio.2021.148415

Title: Photogeneration and reactivity of flavin anionic semiquinone in a bifurcating electron transfer flavoprotein

Journal Article · Thu Jul 01 00:00:00 EDT 2021 · Biochimica et Biophysica Acta - Bioenergetics

DOI:https://doi.org/10.1016/j.bbabio.2021.148415· OSTI ID:1874605

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Electron transfer bifurcation allows production of a strongly reducing carrier at the expense of a weaker one, by redistributing energy among a pair of electrons. Thus, two weakly-reducing electrons from NADH are consumed to produce a strongly reducing ferredoxin or flavodoxin, paid for by reduction of an oxidizing acceptor. The prevailing mechanism calls for participation of a strongly reducing flavin semiquinone which has been difficult to observe with site-certainly in multi-flavin systems. Here, using blue light (450 nm) to photoexcite the flavins of bifurcating electron transfer flavoprotein (ETF), we demonstrate accumulation of anionic flavin semiquinone in excess of what is observed in equilibrium titrations, and establish its ability to reduce the low-potential electron acceptor benzyl viologen. This must occur at the bifurcating flavin because the midpoint potentials of the electron transfer (ET) flavin are not sufficiently negative. We show that bis-tris propane buffer is an effective electron donor to the flavin photoreduction, but that if the system is prepared with the ET flavin chemically reduced, so that only the bifurcating flavin is oxidized and photochemically active, flavin anionic semiquinone is formed more rapidly. Thus, excited bifurcating flavin is able to draw on an electron stored at the ET flavin. Flavin semiquinone photogenerated at the bifurcation site must therefore be accompanied by additional semiquinone formation by oxidation of the ET flavin. Consistent with the expected instability of bifurcating flavin semiquinone, it subsides immediately upon cessation of illumination. However comparison with yields of semiquinone in equilibrium titrations suggest that during continuous illumination at pH 9 a steady state population of 0.3 equivalents of bifurcating flavin semiquinone accumulates, and then undergoes further photoreduction to the hydroquinone. Although transient, the population of bifurcating flavin semiquinone explains the system's ability to conduct light-driven electron transfer from bis-tris propane to benzyl viologen, in effect trapping energy from light.

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Research Organization:: Univ. of Kentucky, Lexington, KY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)

Grant/Contract Number:: SC0021283; CHE-1808433

OSTI ID:: 1874605

Alternate ID(s):: OSTI ID: 1782738; OSTI ID: 1784510

Journal Information:: Biochimica et Biophysica Acta - Bioenergetics, Journal Name: Biochimica et Biophysica Acta - Bioenergetics Vol. 1862 Journal Issue: 7; ISSN 0005-2728

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Title: Photogeneration and reactivity of flavin anionic semiquinone in a bifurcating electron transfer flavoprotein

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