An Unexpected Water Channel in the Light-Harvesting Complex of a Diatom: Implications for the Switch between Light Harvesting and Photoprotection

Many important processes in cells depend on the transfer of protons through water wires embedded in transmembrane proteins. Herein, we have performed more than 55 μs all-atom simulations of the light-harvesting complex of a diatom, i.e., the fucoxanthin and chlorophyll a/c binding protein (FCP) from the marine diatom Phaeodactylum tricornutum. Diatoms are unique models to study natural photosynthesis as they exert an efficient light-harvesting machinery with a robust pH-dependent photoprotective mechanism. The present study reports on the dynamics of an FCP monomer, a dimer, and a tetramer at varying pH values. Surprisingly, we have identified at low pH a water channel across FCP that selectively hydrates and protonates the acrylate of a Chl-c2 pigment located in the middle of the membrane. These results are further supported by QM/MM calculations and steered MD simulations on the proton dynamics. It is shown that proton hopping events between the lumenal and stromal sides of the membrane through the observed water channel are highly disfavored. This hindrance is due to the presence of residues Arg31 and Lys82 close to the acrylate, along with an hydronium desolvation penalty that shows close similarities to the water conductance in aquaporins. Furthermore, we provide strong evidence that this identified water channel is governing the transition between light-harvesting and photoprotective states of the major FCP complex in the diatom P. tricornutum.