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J. Biol. Chem., Vol. 283, Issue 37, 25218-25226, September 12, 2008

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The Thermodynamics and Kinetics of Electron Transfer between Cytochrome b₆f and Photosystem I in the Chlorophyll d-dominated Cyanobacterium, Acaryochloris marina^*

Benjamin Bailleul, Xenie Johnson, Giovanni Finazzi, James Barber, Fabrice Rappaport¹, and Alison Telfer²

From the Institut de Biologie Physico-Chimique, UMR 7141 CNRS-Université Paris 6, 13 Rue Pierre et Marie Curie, Paris 75005, France and the Division of Molecular Biosciences, Imperial College London, Biochemistry Building, South Kensington Campus, London SW7 2AZ, United Kingdom

We have investigated the photosynthetic properties of Acaryochloris marina, a cyanobacterium distinguished by having a high level of chlorophyll d, which has its absorption bands shifted to the red when compared with chlorophyll a. Despite this unusual pigment content, the overall rate and thermodynamics of the photosynthetic electron flow are similar to those of chlorophyll a-containing species. The midpoint potential of both cytochrome f and the primary electron donor of photosystem I (P₇₄₀) were found to be unchanged with respect to those prevailing in organisms having chlorophyll a, being 345 and 425 mV, respectively. Thus, contrary to previous reports (Hu, Q., Miyashita, H., Iwasaki, I. I., Kurano, N., Miyachi, S., Iwaki, M., and Itoh, S. (1998) Proc. Natl. Acad. Sci. U. S. A. 95, 13319–13323), the midpoint potential of the electron donor P₇₄₀ has not been tuned to compensate for the decrease in excitonic energy in A. marina and to maintain the reducing power of photosystem I. We argue that this is a weaker constraint on the engineering of the oxygenic photosynthetic electron transfer chain than preserving the driving force for plastoquinol oxidation by P₇₄₀, via the cytochrome b₆f complex. We further show that there is no restriction in the diffusion of the soluble electron carrier between cytochrome b₆f and photosystem I in A. marina, at variance with plants. This difference probably reflects the simplified ultrastructure of the thylakoids of this organism, where no segregation into grana and stroma lamellae is observed. Nevertheless, chlorophyll fluorescence measurements suggest that there is energy transfer between adjacent photosystem II complexes but not from photosystem II to photosystem I, indicating spatial separation between the two photosystems.

Received for publication, April 21, 2008 , and in revised form, July 16, 2008.

^* This work was supported by the Biotechnology and Biological Science Research Council, United Kingdom, and by CNRS and Université Pierre et marie Curie, Paris 6. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence may be addressed. Tel.: 33-1-5841-5059; E-mail: Fabrice.Rappaport{at}ibpc.fr. ² To whom correspondence may be addressed. Tel.: 44-20-759-41774; E-mail: a.telfer{at}imperial.ac.uk.

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