Interactions among the Photosystem II oxygen-forming complexes: A novel model for damping of O₂ oscillations

It is commonly assumed that the oxygen-evolving centers (OEC's) of PS II operate independently, meaning that there is no transfer of charge among adjacent units, and therefore, that in order to evolve an oxygen molecule each such OEC has to accumulate four charges, as it progresses through the 'S_n' states. This assumption predicts that when a dark-adapted photosynthetic system is exposed to a series of single turnover flashes, the oxygen yield following the third flash will be the product of the fractions of the population of OEC's hit by each of these flashes, and of their initial distribution of S-states. Indeed, measurements with the chlorophyte Chlorella vulgaris and the diatom Phaeodactylum tricornutum show that their oxygen centers are independent, theformer as expected from previous measurements, and predicted by standard theory. However, by this criterion, the centers of the cyanobacterium Synechococcus leopoliensis are not independent. Moreover, in S. leopoliensis the apparent cross-sections derived from the saturation curves for the individual flashes differ from each other, whereas in the former two species, they are constant. Another criterion of independence is the extent of coherency in the Joliot-Kok (period four) oscillations of the flash yield of oxygen. The more independent the OEC's are, the more these oscillations will persist. If the charge flows through a common pool, as in hydrogen formation, the (period two) oscillations are rapidly damped out. By this criterion S. leopoliensis again differs from the classic Chlorella pattern, since the oscillations in this cyanobacterium are rapidly damped. S. leopoliensis differs from Chlorella in additional parameters: oxygen is maximal on the fourth, not the third, flash and oxygen is formed on the very first flash irrespective of the length of dark adaptation. We propose a new model integrating and quantitatively explaining these observations, by allowing 30% of the oxygen-forming centers in S. leopoliensis to exchange charge. A different dark-state distribution of the S-states, maximal at S₀, is also required. The possibility of charge exchange in other systems is discussed.