Evolution of photosynthesis and oxygen evolution: Implications from the structural comparison of Photosystems I and II

Abstract

Two large membrane protein complexes, Photosystem I and II (PS I and PS II), perform the first step in the conversion of the light energy from the sun into chemical energy: the light-induced transmembrane charge separation. They function in series; PS II provides the strong positive redox potential for water oxidation, while PS I generates a strong negative redox potential, which makes it able to reduce ferredoxin and deliver the electrons for the reduction of hydrogen in the form of NADPH. The structural comparison of PS I and PS II sheds light on the evolution of oxygenic photosynthesis. Both Photosystems show similarities in their core structure, indicating that they have been derived from a common ancestor. Striking differences in the arrangement and coordination of cofactors and in their protein environment, however, may contain the secret to the functional differences between the Photosystems. In this article, we address how the oxygen-evolving complex may have developed, and the main similarities and differences in the electron carriers and the organization of the antenna systems of these two complexes.

Structure of cyanobacterial Photosystem I

“…Parts of the peripheral antenna system show homology to the antenna system of PS II (Grotjohann et al 2004), whereas the central domain is specific to PS I and does not exist in PS II. The other striking, unique feature of the antenna system in PS I is the fact that the reaction center domain, i.e.…”

“…The reaction center core shows some similarity to the arrangement of the L and M proteins in bacterial reaction centers (Deisenhofer et al 1984(Deisenhofer et al , 1995Lancaster and Michel 1999) and the D1 and D2 proteins in Photosystem II (Zouni et al 2001;Kamiya and Shen 2003;Ferreira et al 2004;Grotjohann et al 2004). However, the arrangement of type II RCs resembles a more open ''S-shaped'' conformation whereas the 5 C-terminal helices surround the ET chain in PS I like a fence (Grotjohann et al 2004).…”

“…However, the arrangement of type II RCs resembles a more open ''S-shaped'' conformation whereas the 5 C-terminal helices surround the ET chain in PS I like a fence (Grotjohann et al 2004). The similarity between the RC cores supports the idea that all photoreaction centers evolved from a common ancestor and that the genes for PsaA and PsaB evolved by a gene fusion of an ancient RC protein containing five transmembrane helices and an antenna protein consisting of six transmembrane helices, as suggested earlier (Schubert et al 1998).…”

Magnetic field dependence of13C photo-CIDNP MAS NMR in plant photosystems I and II

“…PSI belongs to type I RCs, characterized by three iron-sulfur [4Fe-3S] clusters as terminal intrinsic electron acceptors, while PSII betongs to the type II RCs, where a mobile quinone acts as terminal electron acceptor. The primary donors of both RCs differ in their redox potential by about 700 mV [1]. The oxidized primary electron donor of PSII, P680 " § is the strongest oxidizing agent known in living nature, having a redox potential of 1.2 V [2].…”

Dynamics of electron transfer in photosystem II

“…These investigations have shown a strong similarity between the spatial structure of the PSII and that of the bacterial reaction center [25][26][27]35]. The comparative studies on the similarity of the crystal structure of PSII and of bacterial reaction center and many other biochemical, biophysical, and genetic investigations on the behavior of PSII under different external conditions have contributed to the understanding of the electron and proton transfer within PSII [3,45] but the whole picture of this phenomenon is still missing. For example, we do not know how the primary and secondary electron transfer processes leading to water oxidation are related to each other.…”