TY - JOUR
T1 - Structure, ligands and substrate coordination of the oxygen-evolving complex of photosystem II in the S2 state
T2 - A combined EPR and DFT study
AU - Lohmiller, Thomas
AU - Krewald, Vera
AU - Navarro, Montserrat Pérez
AU - Retegan, Marius
AU - Rapatskiy, Leonid
AU - Nowaczyk, Marc M.
AU - Boussac, Alain
AU - Neese, Frank
AU - Lubitz, Wolfgang
AU - Pantazis, Dimitrios A.
AU - Cox, Nicholas
PY - 2014/6/28
Y1 - 2014/6/28
N2 - The S2 state of the oxygen-evolving complex of photosystem II, which consists of a Mn4O5Ca cofactor, is EPR-active, typically displaying a multiline signal, which arises from a ground spin state of total spin ST = 1/2. The precise appearance of the signal varies amongst different photosynthetic species, preparation and solvent conditions/compositions. Over the past five years, using the model species Thermosynechococcus elongatus, we have examined modifications that induce changes in the multiline signal, i.e. Ca2+/Sr2+- substitution and the binding of ammonia, to ascertain how structural perturbations of the cluster are reflected in its magnetic/electronic properties. This refined analysis, which now includes high-field (W-band) data, demonstrates that the electronic structure of the S2 state is essentially invariant to these modifications. This assessment is based on spectroscopies that examine the metal centres themselves (EPR, 55Mn-ENDOR) and their first coordination sphere ligands ( 14N/15N- and 17O-ESEEM, -HYSCORE and -EDNMR). In addition, extended quantum mechanical models from broken-symmetry DFT now reproduce all EPR, 55Mn and 14N experimental magnetic observables, with the inclusion of second coordination sphere ligands being crucial for accurately describing the interaction of NH3 with the Mn tetramer. These results support a mechanism of multiline heterogeneity reported for species differences and the effect of methanol [Biochim. Biophys. Acta, Bioenerg., 2011, 1807, 829], involving small changes in the magnetic connectivity of the solvent accessible outer MnA4 to the cuboidal unit Mn3O3Ca, resulting in predictable changes of the measured effective 55Mn hyperfine tensors. Sr2+ and NH3 replacement both affect the observed 17O-EDNMR signal envelope supporting the assignment of O5 as the exchangeable μ-oxo bridge and it acting as the first site of substrate inclusion.
AB - The S2 state of the oxygen-evolving complex of photosystem II, which consists of a Mn4O5Ca cofactor, is EPR-active, typically displaying a multiline signal, which arises from a ground spin state of total spin ST = 1/2. The precise appearance of the signal varies amongst different photosynthetic species, preparation and solvent conditions/compositions. Over the past five years, using the model species Thermosynechococcus elongatus, we have examined modifications that induce changes in the multiline signal, i.e. Ca2+/Sr2+- substitution and the binding of ammonia, to ascertain how structural perturbations of the cluster are reflected in its magnetic/electronic properties. This refined analysis, which now includes high-field (W-band) data, demonstrates that the electronic structure of the S2 state is essentially invariant to these modifications. This assessment is based on spectroscopies that examine the metal centres themselves (EPR, 55Mn-ENDOR) and their first coordination sphere ligands ( 14N/15N- and 17O-ESEEM, -HYSCORE and -EDNMR). In addition, extended quantum mechanical models from broken-symmetry DFT now reproduce all EPR, 55Mn and 14N experimental magnetic observables, with the inclusion of second coordination sphere ligands being crucial for accurately describing the interaction of NH3 with the Mn tetramer. These results support a mechanism of multiline heterogeneity reported for species differences and the effect of methanol [Biochim. Biophys. Acta, Bioenerg., 2011, 1807, 829], involving small changes in the magnetic connectivity of the solvent accessible outer MnA4 to the cuboidal unit Mn3O3Ca, resulting in predictable changes of the measured effective 55Mn hyperfine tensors. Sr2+ and NH3 replacement both affect the observed 17O-EDNMR signal envelope supporting the assignment of O5 as the exchangeable μ-oxo bridge and it acting as the first site of substrate inclusion.
UR - http://www.scopus.com/inward/record.url?scp=84901746532&partnerID=8YFLogxK
U2 - 10.1039/c3cp55017f
DO - 10.1039/c3cp55017f
M3 - Article
SN - 1463-9076
VL - 16
SP - 11877
EP - 11892
JO - Physical Chemistry Chemical Physics
JF - Physical Chemistry Chemical Physics
IS - 24
ER -