Surface charge dynamics in photosynthetic membranes and the structural consequences

The strict stacking of plant photosynthetic membranes into granal structures plays a vital role in energy conversion. The molecular forces that lead to grana stacking, however, are poorly understood. Here we evaluate the interplay between repulsive electrostatic (F_el) and attractive van der Waals (F_vdWaals) forces in grana stacking. In contrast to previous reports, we find that the physicochemical balance between attractive and repulsive forces fully explains grana stacking. Extending the force balance analysis to lateral interactions within the oxygen-evolving photosystem II (PSII)-light harvesting complex II (LHCII) supercomplex reveals that supercomplex stability is very sensitive to F_el changes. F_el is highly dynamic, increasing up to 1.7-fold on addition of negative charges by phosphorylation of grana-hosted proteins. We show that this leads to specific destabilization of the supercomplex, and that changes in F_el have contrasting effects on vertical stacking and lateral intramembrane organization. This enables discrete biological control of these central structural features.