Laser-Flash Kinetic Analysis of the Fast Electron Transfer from Plastocyanin and Cytochrome c6 to Photosystem I. Experimental Evidence on the Evolution of the Reaction Mechanism

Abstract

The reaction mechanism of electron transfer from the interchangeable metalloproteins plastocyanin (Pc) and cytochrome c6 (Cyt) to photooxidized P700 in photosystem I (PSI) has been studied by laser-flash absorption spectroscopy using a number of evolutionarily differentiated organisms such as cyanobacteria (Anabaena sp. PCC 7119 and Synechocystis sp. PCC 6803), green algae (Monoraphidium braunii), and higher plants (spinach). PSI reduction by Pc or Cyt shows different kinetics depending on the organism from which the photosystem and metalloproteins are isolated. According to the experimental data herein reported, three different kinetic models are proposed by assuming either an oriented collisional reaction mechanism (type I), a minimal two-step mechanism involving complex formation followed by intracomplex electron transfer (type II), or rearrangement of the reaction partners within the complex before electron transfer takes place (type III). Our findings suggest that PSI was able to first optimize its interaction with positively charged Cyt and that the evolutionary replacement of the ancestral Cyt by Pc, as well as the appearance of the fast kinetic phase in the Pc/PSI system of higher plants, would involve structural modifications in both the donor protein and PSI.

The Interactions of Cyanobacterial Cytochromec6 and Cytochrome f, Characterized by NMR

“…This functional convergence suggests that similar interaction properties exist for both proteins. Not surprisingly, Pc and cytc 6 have comparable redox potentials of around 350 mV. Furthermore, both proteins provide similar recognition information, demonstrated by the parallel variation of their isoelectric points, being acidic in green algae while ranging from acidic to basic in cyanobacteria (1,4,5).…”

“…In plants, this task is fulfilled by plastocyanin (Pc), whereas cytochrome c 6 (cytc 6 ) is the only carrier in certain cyanobacteria. There also exist eukaryotic algae and cyanobacteria, which have the capacity to replace Pc with cytc 6 under copper-depleted conditions (1). Recently, a cytc 6 -like protein has been discovered in the thylakoid lumen of Arabidopsis (2,3).…”

“…There also exist eukaryotic algae and cyanobacteria, which have the capacity to replace Pc with cytc 6 under copper-depleted conditions (1). Recently, a cytc 6 -like protein has been discovered in the thylakoid lumen of Arabidopsis (2,3). Despite being evolutionarily unrelated, Pc and cytc 6 perform equivalent tasks with common reaction partners.…”

“…Recently, a cytc 6 -like protein has been discovered in the thylakoid lumen of Arabidopsis (2,3). Despite being evolutionarily unrelated, Pc and cytc 6 perform equivalent tasks with common reaction partners. This functional convergence suggests that similar interaction properties exist for both proteins.…”

“…To date there has been a considerable amount of kinetic and mutational analysis of the electron transfer reaction between both Pc and cytc 6 and their partner PSI (6 -11). A hierarchy of mechanisms for interprotein electron transport has emerged from this work.…”