Single-molecule study of redox control involved in establishing the spinach plastocyanin-cytochrome b6f electron transfer complex

Mayneord, Guy E., Vasilev, Cvetelin, Malone, Lorna A., Swainsbury, David J.K., Hunter, C. Neil and Johnson, Matthew P. (2019) Single-molecule study of redox control involved in establishing the spinach plastocyanin-cytochrome b6f electron transfer complex. Biochimica et Biophysica Acta - Bioenergetics, 1860 (7). pp. 591-599. ISSN 0005-2728

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Abstract

Small diffusible redox proteins play a ubiquitous role in bioenergetic systems, facilitating electron transfer (ET) between membrane bound complexes. Sustaining high ET turnover rates requires that the association between extrinsic and membrane-bound partners is highly specific, yet also sufficiently weak to promote rapid post-ET separation. In oxygenic photosynthesis the small soluble electron carrier protein plastocyanin (Pc) shuttles electrons between the membrane integral cytochrome b6f (cytb6f) and photosystem I (PSI) complexes. Here we use peak-force quantitative nanomechanical mapping (PF-QNM) atomic force microscopy (AFM) to quantify the dynamic forces involved in transient interactions between cognate ET partners. An AFM probe functionalised with Pc molecules is brought into contact with cytb6f complexes, immobilised on a planar silicon surface. PF-QNM interrogates the unbinding force of the cytb6f-Pc interactions at the single molecule level with picoNewton force resolution and on a time scale comparable to the ET time in vivo (ca. 120 μs). Using this approach, we show that although the unbinding force remains unchanged the interaction frequency increases over five-fold when Pc and cytb6f are in opposite redox states, so complementary charges on the cytb6f and Pc cofactors likely contribute to the electrostatic forces that initiate formation of the ET complex. These results suggest that formation of the docking interface is under redox state control, which lowers the probability of unproductive encounters between Pc and cytb6f molecules in the same redox state, ensuring the efficiency and directionality of this central reaction in the ‘Z-scheme’ of photosynthetic ET.

Item Type: Article
Additional Information: Funding Information: M.P.J. and C.N.H gratefully acknowledge funding ( BB/M000265/1 and BB/P002005/1 ) from the Biotechnology and Biological Sciences Research Council (U.K.). C.N.H. also acknowledges financial support from Advanced Award 338895 from the European Research Council . G.E.M. was supported by a doctoral studentship from The Grantham Foundation . This work was also supported as part of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the US Department of Energy , Office of Science , and Office of Basic Energy Sciences under Award Number DE-SC0001035 . PARC's role was to partially fund the Multimode VIII AFM system and to provide partial support for C.N.H. Publisher Copyright: © 2019 Elsevier B.V.
Uncontrolled Keywords: atomic force microscopy,electron transfer, cytochrome b6f,photosynthesis,plastocyanin,biophysics,biochemistry,cell biology ,/dk/atira/pure/subjectarea/asjc/1300/1304
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 17 Aug 2022 12:31
Last Modified: 24 Sep 2022 07:04
URI: https://ueaeprints.uea.ac.uk/id/eprint/87357
DOI: 10.1016/j.bbabio.2019.06.013

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