Photosystem I Reduction in Diatoms: As Complex as the Green Lineage Systems but Less Efficient

Abstract

Diatoms occupy a key branch in the evolutionary tree of oxygen-evolving photosynthetic organisms. Here, the electron transfer reaction mechanism from cytochrome c 6 to photosystem I from the diatom Phaeodactylum tricornutum has been analyzed by laser-flash absorption spectroscopy. Kinetic traces of photosystem I reduction fit to biphasic curves, the analysis of the observed rate constants indicating that electron transfer occurs in a cytochrome c 6 /photosystem I transient complex, which undergoes a reorganization process from the initial encounter complex to the optimized final configuration. The mild ionic strength dependence of the rate constants makes evident the relatively weak electrostatically attractive nature of the interaction. Taken together, these results indicate that the "red" Phaeodactylum system is less efficient than "green" systems, both in the formation of the properly arranged (cytochrome c 6 /photosystem I) complex and in the electron transfer itself. The results obtained from cross-reactions with cytochrome c 6 and photosystem I from cyanobacteria, green algae, and plants shed light on the different evolutionary pathway of the electron transfer to photosystem I in diatoms with regard to the way that it evolved in higher plants.

Interaction of photosystem I from Phaeodactylum tricornutum with plastocyanins as compared with its native cytochrome c6: Reunion with a lost donor

“…Recently, the ET reaction mechanism from Cyt to PSI from the diatom Phaeodactylum tricornutum has been first analyzed by laser-flash absorption spectroscopy [17], indicating that ET occurs within a Cyt/PSI transient complex that undergoes a reorganization process from the initial encounter complex to the optimized final configuration, as already described in "green" PSI systems. However, the results also demonstrated that the "red" Phaeodactylum system possesses a lower efficiency than "green" systems, both in the formation of the properly arranged [Cyt-PSI] complex and in the electron transfer itself [17]. In addition, the relatively weak electrostatically attractive nature of the Cyt/PSI interaction seems to represent a compromise between the efficiency in the ET process and the need for a fast exchange of the protein donor [17].…”

“…However, the results also demonstrated that the "red" Phaeodactylum system possesses a lower efficiency than "green" systems, both in the formation of the properly arranged [Cyt-PSI] complex and in the electron transfer itself [17]. In addition, the relatively weak electrostatically attractive nature of the Cyt/PSI interaction seems to represent a compromise between the efficiency in the ET process and the need for a fast exchange of the protein donor [17].…”

“…PSI particles from the diatom P. tricornutum were obtained by β-dodecyl-maltoside (β-DM) solubilization as previously described [17]. Pcs from the cyanobacterium Nostoc sp.…”

“…PCC 7119 [23]. Protein purifications from the periplasmic fractions were carried out as previously described [17,21]. Chlamydomonas Pc mutants were generated by site-directed mutagenesis using oligonucleotide pairs containing the sequence change desired (Fig.…”

“…However, PSI from cyanobacteria, where both Pc and Cyt can be acidic, neutral or basic, lacks this extra loop, and thus the role of electrostatic forces in the interaction with PSI varies consequently [13][14][15][16]. By its turn, although the evolution of the electron transfer (ET) to PSI in diatoms has also led to complementary electrostatic interactions between acidic and basic patches in Cyt and the PsaF subunit, respectively, the electrostatic character of both partners is similarly reduced, the intensity of the interaction being accordingly weakened as compared with the strongest electrostatic properties of the Cyt(Pc)/PSI complex in the green lineage [17].…”