Mechanism of Radical Formation in the H‑Bond Network of D1-Asn298 in Photosystem II

In photosystem II (PSII), redox-active tyrosine Z (TyrZ) forms a low-barrier H-bond with Nε of D1-His190. The PSII crystal structures show that Nδ of D1-His190 donates an H-bond to the carbonyl O of D1-Asn298. However, at a level of ∼2 Å resolution, a clear discrimination between the −NH2 and −CO groups of the asparagine side chain may not be possible based on the electron density map. Using quantum mechanical/molecular mechanical calculations, we investigated the energetics of the D1-Asn298 conformations. In the D1-Asn298-rotated conformation, where the amide N group donates an H-bond to deprotonated Nδ of D1-His190, oxidation of S2 resulted in formation of a neutral radical, either TyrZ• or D1-His190•. This suggests that in the D1-Asn298-rotated conformation, the redox potential (Em) values of TyrZ/D1-His190 are lower than the Em of the Mn4CaO5 cluster due to deprotonated D1-His190. The large disorder of a water molecule (water 1117A) at D1-Asn298 in the crystal structure as well as the absence of water 1117A in the Sr2+-substituted crystal structure may be associated with coexistence of the two D1-Asn298 conformations in the crystals.