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Transient Interactions Between Soluble Electron Transfer Proteins. The Case of Plastocyanin and Cytochrome f

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Bioenergetic Processes of Cyanobacteria

Abstract

Oxygenic photosynthesis depends absolutely on electron transfer between cytochrome f and plastocyanin (or cytochrome c 6). The reaction must be very fast if it is not to limit the rate of photosynthesis; it also depends on diffusional interaction between the two proteins. This implies that it is highly transient, and involves specific binding in a configuration that allows rapid electron transfer. The specificity must be strictly limited, however, because high specificity would endanger rapid turnover of the electron transport chain and the promiscuous reactions of plastocyanin with photosystem I and cytochrome oxidase. Reaction of cytochrome f with plastocyanin is an outstanding example of weak, transient protein interactions, which include many signalling systems as well as electron transfer. The structural basis of this type of interaction is not well understood because of the difficulty of obtaining crystal structures for transient complexes. This has been overcome with plastocyanin by using NMR techniques that provide information on both structure and dynamics of the complex. Cyanobacteria provide the most complete information currently available. The aim of this chapter is to present our current understanding of the system in terms of the fundamental physical, structural and kinetic factors that must be satisfied to achieve rapid electron transfer. The overriding consideration is how to achieve an appropriately short distance between redox centers; desolvation of the interface is shown to be a critical factor. Transient, semi-specific binding can the be achieved in many ways. Although complementary electrostatic charges accelerate binding, they do not necessarily result in strong binding, and in some cyanobacteria hydrophobic interactions and hydrophobic channelling largely take over from electrostatics. The above considerations, which have been developed by study of the reaction in solution, help to illuminate the behaviour of the system in vivo and the evolutionary pressures which have shaped it. An important feature of the transition from cyanobacteria to eukaryotic oxyphototrophs has been the loss of cytochrome oxidase from plastids.

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Acknowledgements

Work from our own laboratory has been supported by the Biotechnology and Biological Sciences Research Council, the Oppenheimer Fund, University of Cambridge, and Corpus Christi College, Cambridge. We are grateful to Barry Honig for making available the program Delphi, to Edward Solomon for providing atomic partial charges for the copper center of plastocyanin and to Peter Crowley for providing the coordinates of the complex between cytochrome f and plastocyanin from Phormidium laminosum.

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  1. Department of Biochemistry, University of Cambridge, Downing Site, CB2 1QW, Cambridge, UK

    Derek S. Bendall, Beatrix G. Schlarb-Ridley & Christopher J. Howe

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  1. Derek S. Bendall
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  2. Beatrix G. Schlarb-Ridley
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  3. Christopher J. Howe
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Correspondence to Derek S. Bendall .

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  1. Inst. Physikalische Chemie, Molecular Bioenergetics Group, Univ. Wien, Währingerstr. 42, Wien, 1090, Austria

    Guenter A. Peschek

  2. Department für Chemie, Abteilung für Biochemie, Universität für Bodenkultur Wien, Althanstrasse 14, Wien, 1190, Austria

    Christian Obinger

  3. Fak. II Mathematik/Naturwissenschaften, Institut für Chemie, TU Berlin, Straße des 17. Juni 135, Berlin, 10587, Berlin, Germany

    Gernot Renger

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Bendall, D.S., Schlarb-Ridley, B.G., Howe, C.J. (2011). Transient Interactions Between Soluble Electron Transfer Proteins. The Case of Plastocyanin and Cytochrome f . In: Peschek, G., Obinger, C., Renger, G. (eds) Bioenergetic Processes of Cyanobacteria. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0388-9_19

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