TY - JOUR
T1 - Hydration preferences for Mn4Ca cluster models of photosystem II
T2 - Location of potential substrate-water binding sites
AU - Petrie, Simon
AU - Stranger, Rob
AU - Pace, Ron J.
PY - 2010/12/17
Y1 - 2010/12/17
N2 - Density functional theory calculations are reported on a set of three model structures of the Mn4Ca cluster in the water-oxidizing complex of Photosystem II (PSII), which share the structural formula [CaMn 4C9H10N2O16] q+•(H2O)n (q=-1, 0, 1, 2, 3; n=0-7). In these calculations we have explored the preferred hydration sites of the Mn 4Ca cluster across five overall oxidation states (S0 to S4) and all feasible magnetic-coupling arrangements to identify the most likely substrate-water binding sites. We have also explored charge-compensated structures in which the overall charge on the cluster is maintained at q=0 or +1, which is consistent with the experimental data on sequential proton loss in the real system. The three model structures have skeletal arrangements that are strongly reminiscent, in their relative metal-atom positions, of the 2.9-, 3.7-, and 3.5 Å-resolution crystal structures, respectively, whereas the charge states encompassed in our study correspond to an assignment of (MnIII)3MnII for S0 and up to (MnIV)3MnIII for S4. The three models differ principally in terms of the spatial relationship between one Mn (Mn(4)) and a generally robust Mn3Ca tetrahedron that contains Mn(1), Mn(2), and Mn(3). Oxidation-state distributions across the four manganese atoms, in most of the explored charge states, are dependent on details of the cluster geometry, on the extent of assumed hydration of the clusters, and in some instances on the imposed magnetic-coupling between adjacent Mn atoms. The strongest water-binding sites are generally those on Mn(4) and Ca. However, one structure type displays a high-affinity binding site between Ca and Mn(3), the S-state-dependent binding-energy pattern of which is most consistent with the substrate water-exchange kinetics observed in functional PSII. This structure type also permits another water molecule to access the cluster in a manner consistent with the substrate-water interaction with the Mn cluster, seen in electron spin-echo envelope modulation (ESEEM) studies of the functional enzyme in the S0 and S2 states. It also rationalizes the significant differences in hydrogen-bonding interactions of the substrate water observed in the FTIR measurements of the S1 and S2 states. We suggest that these two water-binding sites, which are molecularly close, model the actual substrate-binding sites in the enzyme. Water ways: Density functional calculations are reported on a set of three model structures of the Mn4Ca cluster in the water-oxidizing complex of Photosystem II (see figure). The preferred hydration sites across five oxidation states and all feasible magnetic-coupling arrangements have been explored to identify the most likely substrate-water binding sites.
AB - Density functional theory calculations are reported on a set of three model structures of the Mn4Ca cluster in the water-oxidizing complex of Photosystem II (PSII), which share the structural formula [CaMn 4C9H10N2O16] q+•(H2O)n (q=-1, 0, 1, 2, 3; n=0-7). In these calculations we have explored the preferred hydration sites of the Mn 4Ca cluster across five overall oxidation states (S0 to S4) and all feasible magnetic-coupling arrangements to identify the most likely substrate-water binding sites. We have also explored charge-compensated structures in which the overall charge on the cluster is maintained at q=0 or +1, which is consistent with the experimental data on sequential proton loss in the real system. The three model structures have skeletal arrangements that are strongly reminiscent, in their relative metal-atom positions, of the 2.9-, 3.7-, and 3.5 Å-resolution crystal structures, respectively, whereas the charge states encompassed in our study correspond to an assignment of (MnIII)3MnII for S0 and up to (MnIV)3MnIII for S4. The three models differ principally in terms of the spatial relationship between one Mn (Mn(4)) and a generally robust Mn3Ca tetrahedron that contains Mn(1), Mn(2), and Mn(3). Oxidation-state distributions across the four manganese atoms, in most of the explored charge states, are dependent on details of the cluster geometry, on the extent of assumed hydration of the clusters, and in some instances on the imposed magnetic-coupling between adjacent Mn atoms. The strongest water-binding sites are generally those on Mn(4) and Ca. However, one structure type displays a high-affinity binding site between Ca and Mn(3), the S-state-dependent binding-energy pattern of which is most consistent with the substrate water-exchange kinetics observed in functional PSII. This structure type also permits another water molecule to access the cluster in a manner consistent with the substrate-water interaction with the Mn cluster, seen in electron spin-echo envelope modulation (ESEEM) studies of the functional enzyme in the S0 and S2 states. It also rationalizes the significant differences in hydrogen-bonding interactions of the substrate water observed in the FTIR measurements of the S1 and S2 states. We suggest that these two water-binding sites, which are molecularly close, model the actual substrate-binding sites in the enzyme. Water ways: Density functional calculations are reported on a set of three model structures of the Mn4Ca cluster in the water-oxidizing complex of Photosystem II (see figure). The preferred hydration sites across five oxidation states and all feasible magnetic-coupling arrangements have been explored to identify the most likely substrate-water binding sites.
KW - density functional calculations
KW - metalloproteins
KW - mixed-valent compounds
KW - photosystem II
KW - water chemistry
UR - http://www.scopus.com/inward/record.url?scp=78650270001&partnerID=8YFLogxK
U2 - 10.1002/chem.201001132
DO - 10.1002/chem.201001132
M3 - Article
SN - 0947-6539
VL - 16
SP - 14026
EP - 14042
JO - Chemistry - A European Journal
JF - Chemistry - A European Journal
IS - 47
ER -