Control of electron transport in photosystem I by the iron-sulfur cluster F_x in response to intra- and intersubunit interactions

Photosystem I (PS I) is a transmembraneal multisub-unit complex that mediates light-induced electron transfer from plactocyanine to ferredoxin. The electron transfer proceeds from an excited chlorophyll a dimer (P700) through a chlorophyll a (A₀), a phylloquinone (A₁), and a [4Fe-4S] iron-sulfur cluster F_x, all located on the core subunits PsaA and PsaB, to iron-sulfur clusters F_A and F_B, located on subunit PsaC. Earlier, it was attempted to determine the function of F_x in the absence of F_A/B mainly by chemical dissociation of subunit PsaC. However, not all PsaC subunits could be removed from the PS I preparations by this procedure without partially damaging F_x. We therefore removed subunit PsaC by interruption of the psaC2 gene of PS I in the cyanobacterium Synechocystis sp. PCC 6803. Cells could not grow under photosynthetic conditions when subunit PsaC was deleted, yet the PsaC-deficient mutant cells grew under heterotrophic conditions and assembled the core subunits of PS I in which light-induced electron transfer from P700 to A₁ occurred. The photoreduction of F_x was largely inhibited, as seen from direct measurement of the extent of electron transfer from A₁ to F_x. From the crystal structure it can be seen that the removal of subunits PsaC, PsaD, and PsaE in the PsaC-deficient mutant resulted in the braking of salt bridges between these subunits and PsaB and PsaA and the formation of a net of two negative surface charges on PsaA/B. The potential induced on F_x by these surface charges is proposed to inhibit electron transport from the quinone. In the complete PS I complex, replacement of a cysteine ligand of F_x by serine in site-directed mutation C565S/D566E in subunit PsaB caused an ∼10-fold slow down of electron transfer from the quinone to F_x without much affecting the extent of this electron transfer compared with wild type. Based on these and other results, we propose that F_x might have a major role in controlling electron transfer through PS I.