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

Photosystem I (PS I) is a transmembraneal multisubunit 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 (A(0)), a phylloquinone (A(1)), 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 A(1) occurred. The photoreduction of F-X was largely inhibited, as seen from direct measurement of the extent of electron transfer from A(1) 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 similar to10-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.