Oxidation of water molecules in the photosystem II (PSII) protein complex
proceeds at the manganese–calcium complex, which is buried deeply in the
lumenal part of PSII. Understanding the PSII function requires knowledge of
the intricate coupling between the water-oxidation chemistry and the dynamic
proton management by the PSII protein matrix. Here we assess the structural
basis for long-distance proton transfer in the interior of PSII and for proton
management at its surface. Using the recent high-resolution crystal structure
of PSII, we investigate prominent hydrogen-bonded networks of the lumenal side
of PSII. This analysis leads to the identification of clusters of polar groups
and hydrogen-bonded networks consisting of amino acid residues and water
molecules. We suggest that long-distance proton transfer and conformational
coupling is facilitated by hydrogen-bonded networks that often involve more
than one protein subunit. Proton-storing Asp/Glu dyads, such as the
D1-E65/D2-E312 dyad connected to a complex water-wire network, may be
particularly important for coupling protonation states to the protein
conformation. Clusters of carboxylic amino acids could participate in proton
management at the lumenal surface of PSII. We propose that rather than having
a classical hydrophobic protein interior, the lumenal side of PSII resembles a
complex polyelectrolyte with evolutionary optimized hydrogen-bonding networks.
This article is part of a Special Issue entitled: Photosynthesis Research for
Sustainability: from Natural to Artificial