Oxygen-evolving complex of Photosystem II: an analysis of second-shell residues and hydrogen-bonding networks

Abstract

The oxygen-evolving complex (OEC) is a Mn4O5Ca cluster embedded in the Photosystem II (PSII) protein complex. As the site of water oxidation, the OEC is connected to the lumen by channels that conduct water, oxygen, and/or protons during the catalytic cycle. The hydrogen-bond networks found in these channels also serve to stabilize the oxidized intermediates, known as the S states. We review recent developments in characterizing these networks via protein mutations, molecular inhibitors, and computational modeling. On the basis of these results, we highlight regions of the PSII protein in which changes have indirect effects on the S1, S2, and S3 oxidation states of the OEC while still allowing photosynthetic activity.

Substitution of the D1-Asn87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II

“…Spinach PSII membranes were prepared as described previously (61,62) 2 ], and MES (pH 6.5). Oxygen evolution was monitored with a Clarktype electrode, and the oxygen-assay chamber was maintained at 25 °C using a temperaturecontrolled water bath.…”

“…The site of water oxidation, known as the oxygen-evolving complex (OEC), consists of a µ-oxo-bridged tetramanganese-calcium cluster ligated by a number of amino-acid residues and water molecules (1). The OEC is surrounded by a network of hydrogen-bonded amino-acid residues and water molecules that, along with Cl -ions, play a pivotal role in water oxidation (2,3). This process is initiated by photoinduced charge separation via a chlorophyll molecule called P 680 .…”

“…Sequence alignment studies of the second-shell residues have revealed that the only statistically significant difference between the two species occurs at the D1-87 site (2). This site is occupied by an asparagine residue in a significant majority of cyanobacterial PSII including Synechocystis PCC 6803 as opposed to an alanine residue in spinach PSII.…”

“…This site is occupied by an asparagine residue in a significant majority of cyanobacterial PSII including Synechocystis PCC 6803 as opposed to an alanine residue in spinach PSII. Furthermore, this residue is an important part of the "narrow" channel of hydrogen-bonded waters whose role is yet to be determined (2). The hydrogen-bonding network surrounding the Mn cluster is extensive; therefore, perturbation at any point might be propagated over a long distance and can affect remote sites like the Cl --binding site which is about 13 Å from the D1-87 residue.…”

Gernot Renger (1937–2013): his life, Max-Volmer Laboratory, and photosynthesis research

“…In addition, the direct ligands were included, and recently many have realized that the second and third sphere ligands, as well as structural water molecules, are also essential for the catalytic efficiency of the enzyme. Collectively, this environment forms the hydrogen-bonding network that allows removal of protons from the active site, which is very important for water splitting (Umena et al 2011;Renger 2012;Debus 2015;Vogt et al 2015). Interestingly, Renger (1977b) had already discussed various aspects of proton release from the catalytic site, including the possible effects of the protein matrix on it.…”