Dynamic Coupling and Disorder in Aggregation of Light-Harvesting Complex II in Plant Thylakoid Membranes.

The dynamics of the aggregated light-harvesting complex (LHCII) associated with its antenna pigments can be crucial for a transition between light-harvesting and dissipative states, which is pivotal for nonphotochemical quenching (NPQ). To this end, aggregation of pigment-binding LHCII monomers and PsbS-associated trimers in neutral and low lumenal pH respectively, has been investigated when embedded in the plant thylakoid membranes, using coarse-grained molecular dynamics simulations. Both pigment-binding LHCII monomers and PsbS-associated trimers dynamically form and break dimers and higher-order aggregates in thylakoids within the simulation time. During aggregation of the monomeric and the PsbS-associated trimeric LHCII, survival probability representing conformations of the N-terminus, helices, and the respective antennae pigments follows a nonexponential decay with multiple residence time scales. The dimer residence time of the trimers at low lumenal pH is higher than that of the monomers at neutral pH. The conformational fluctuations of the proteins occur under a fast fluctuation limit in the presence of slower interpigment distance fluctuations, highlighting the presence of disorder in LHCII for both monomeric and trimeric LHCII aggregations in neutral and low lumenal pH. The multiple residence times lead to a time-dependent rate, unlike conventional rate theory. As the rate becomes a stochastic function of time, disorder emerges. Thus, LHCII aggregation does not proceed through a single uniform pathway. Instead, it involves a range of coupled dynamics, with some contacts forming and breaking with various time scales and transitions among multistates originating from dimer, trimer, and higher-order aggregates in thylakoids relevant for regulating NPQ.