BioPHYSICAL chemistry

between two manganese atoms, other than
the bridged manganese. In addition, a peak
at 3.4 Å was assigned as representing a
manganese-to-calcium distance. The shortest
distances are from manganese ligands to
oxygen and nitrogen, which cannot be
resolved in these measurements. Based upon
these distances a wide array of possible
arrangements for the manganese cluster were
possible. Although the possible configurations
still remain open, the combination of the
EXAFS, EPR, and X-ray data is most con-
sistent with an asymmetric configuration
with one manganese being somewhat distant
from the other three.
As the manganese cluster becomes more
oxidized, the positive charges could become
very destabilizing. Since the cluster has four
manganese, the charges can be distributed
over the cluster to minimize any unfavor-
able oxidation state of any single manganese
but the site would still be gaining charge.
Mechanisms that increase the oxidation of the
cluster would require bond rearrangements of the cluster that would
trigger the water oxidation but such bond changes were not supported
by the spectroscopic studies.
These difficulties were largely resolved with the development of the
hydrogen-abstraction model, which invoked a direct involvement of
the tyrosyl radical in both the electron and proton transfers. Consider
a simple model which places YZ in close proximity to the manganese
clusterwith a bound water molecule (Figure 20.15). Light excitation
causes formation of P680+(Figure 20.15a), which is rapidly reduced by
YZ(Figure 20.15b) with a coupled release of the phenolic proton to a nearby
base (Figure 20.15c). The proton does not stay at the base but leaves as
the base is part of a proton pathway to the luminal surface (Figure 20.15d).
The S-state advancement occurs as the electron is transferred from YZ
to the manganese cluster, leaving a strong tyrosine base (Figure 20.15e).
The tyrosine base abstracts a proton from the bound water molecule
(Figure 20.15f), leaving a hydroxyl group bound to the manganese
cluster. The tyrosine is then reset allowing the second proton to be
abstracted after the next excitation of P680. By including a direct role of
YZin the process, electron and proton transfer are naturally coupled together
in a manner that drives water oxidation. Since a proton is transferred
away from the manganese cluster after each oxidation step, the overall
charge of the cluster does not change during the S cycles.

CHAPTER 20 PHOTOSYNTHESIS 435

0246

FT amplitude

Distance (Å)

Mn-ligand

1.8Å

Mn-Mn

2.7Å

Mn-Mn

Mn-Ca

3.4Å

Figure 20.14EXAFS spectrum of photosystem II

revealing the distances in the Mn cluster. Modified

from Yano et al. (2006).